diff --git a/BUILD.gn b/BUILD.gn
index c1179533453..f8411f94213 100644
--- a/BUILD.gn
+++ b/BUILD.gn
@@ -61,6 +61,7 @@ group("runtime") {
     deps += [
       "runtime/bin:dartaotruntime",
       "runtime/bin:dartaotruntime_product",
+      "utils/dart_runtime_service_vm",
       "utils/dart_runtime_service_vm:dart_runtime_service_vm_aot_snapshot",
       "utils/dartdev:dartdev_aot_snapshot",
       "utils/dds:dds_aot",
diff --git a/build/rbe/rewrapper_dart.py b/build/rbe/rewrapper_dart.py
index bf172049492..012e990c309 100644
--- a/build/rbe/rewrapper_dart.py
+++ b/build/rbe/rewrapper_dart.py
@@ -360,6 +360,9 @@ trace to find the place to insert the appropriate support.
             elif arg == 'gen/utils/bazel/kernel_worker.dart.dill':
                 self.extra_paths.add(self.rebase(arg))
                 return self.parse_kernel_worker()
+            elif arg == 'gen/utils/dart_runtime_service_vm/generate_dart_runtime_service_vm_snapshot.dart.dill':
+                self.extra_paths.add(self.rebase(arg))
+                return self.parse_generate_dart_runtime_service_vm_snapshot()
             elif arg == 'gen/utils/dartdev/generate_dartdev_snapshot.dart.dill':
                 self.extra_paths.add(self.rebase(arg))
                 return self.parse_generate_dartdev_snapshot()
@@ -677,6 +680,15 @@ trace to find the place to insert the appropriate support.
             else:
                 self.unsupported('kernel_worker', arg)
 
+    def parse_generate_dart_runtime_service_vm_snapshot(self):
+        while self.has_next_arg:
+            arg = self.next_arg()
+            if arg in ['--help']:
+                pass
+            else:
+                self.unsupported('generate_dart_runtime_service_vm_snapshot',
+                                 arg)
+
     def parse_generate_dartdev_snapshot(self):
         while self.has_next_arg:
             arg = self.next_arg()
diff --git a/pkg/dart_runtime_service/lib/dart_runtime_service.dart b/pkg/dart_runtime_service/lib/dart_runtime_service.dart
index 5d7cd085781..0b65a39168a 100644
--- a/pkg/dart_runtime_service/lib/dart_runtime_service.dart
+++ b/pkg/dart_runtime_service/lib/dart_runtime_service.dart
@@ -5,5 +5,7 @@
 export 'src/dart_runtime_service.dart';
 export 'src/dart_runtime_service_backend.dart';
 export 'src/dart_runtime_service_options.dart';
+export 'src/event_streams.dart';
 export 'src/exceptions.dart';
+export 'src/isolate_manager.dart';
 export 'src/rpc_exceptions.dart';
diff --git a/pkg/dart_runtime_service/lib/src/clients.dart b/pkg/dart_runtime_service/lib/src/clients.dart
index 2e8060af345..af9a8062996 100644
--- a/pkg/dart_runtime_service/lib/src/clients.dart
+++ b/pkg/dart_runtime_service/lib/src/clients.dart
@@ -25,7 +25,9 @@ base class Client {
     required UnmodifiableNamedLookup<Client> clients,
     required EventStreamMethods eventStreamMethods,
     required this.backend,
+    String? name,
   }) {
+    _name = name ?? defaultClientName;
     _clientPeer = json_rpc.Peer(connection, strictProtocolChecks: false);
     _internalRpcs = DartRuntimeServiceRpcs(
       clients: clients,
@@ -47,12 +49,15 @@ base class Client {
   late final Future<void> done;
 
   Future<void> initialize({required String namespace}) {
+    logger.info('Initializing...');
     this.namespace = namespace;
     registerRpcHandlers();
     done = _listen().then((_) {
+      logger.info('Client connection closed.');
       // Cleanup stream subscription state when the client disconnects.
       _internalRpcs.eventStreamMethods.onClientDisconnect(this);
     });
+    logger.info('Initialization complete.');
     return done;
   }
 
@@ -64,6 +69,7 @@ base class Client {
   /// Called if the connection to the client should be closed.
   @mustCallSuper
   Future<void> close() async {
+    logger.info('Cleaning up.');
     await _clientPeer.close();
   }
 
@@ -157,8 +163,13 @@ base class Client {
   /// Sets the name associated with this client.
   ///
   /// If [n] is null, the client name is reset to [defaultClientName].
-  void setName(String? n) => _name = n ?? defaultClientName;
-  late String _name = defaultClientName;
+  void setName(String? n) {
+    final updated = n ?? defaultClientName;
+    logger.info('Changing client name to $updated.');
+    _name = updated;
+  }
+
+  late String _name;
 }
 
 /// Used for keeping track and managing clients that are connected to a given
@@ -185,12 +196,13 @@ base class ClientManager {
   ///
   /// This should be called when a client connects to the service.
   @mustCallSuper
-  Client addClient(StreamChannel<String> connection) {
+  Client addClient({required StreamChannel<String> connection, String? name}) {
     final client = Client(
       connection: connection,
       clients: UnmodifiableNamedLookup(clients),
       eventStreamMethods: eventStreamMethods,
       backend: backend,
+      name: name,
     );
     final namespace = clients.add(client);
     client.initialize(namespace: namespace).then((_) {
diff --git a/pkg/dart_runtime_service/lib/src/dart_runtime_service.dart b/pkg/dart_runtime_service/lib/src/dart_runtime_service.dart
index 754883d9ad6..2c5d2319bd4 100644
--- a/pkg/dart_runtime_service/lib/src/dart_runtime_service.dart
+++ b/pkg/dart_runtime_service/lib/src/dart_runtime_service.dart
@@ -3,12 +3,14 @@
 // BSD-style license that can be found in the LICENSE file.
 
 import 'dart:async';
+import 'dart:developer';
 import 'dart:io';
 
 import 'package:logging/logging.dart';
 import 'package:meta/meta.dart';
 import 'package:shelf/shelf.dart' as shelf;
 import 'package:shelf/shelf_io.dart' as io;
+import 'package:stream_channel/stream_channel.dart';
 
 import 'clients.dart';
 import 'dart_runtime_service_backend.dart';
@@ -19,32 +21,43 @@ import 'handlers.dart';
 import 'utils.dart';
 
 typedef RpcResponse = Map<String, Object?>;
+typedef DartRuntimeServiceBackendBuilder =
+    DartRuntimeServiceBackend Function(DartRuntimeService);
 
 class DartRuntimeService {
-  DartRuntimeService._({required this.config, required this.backend})
-    : authCode = config.disableAuthCodes ? null : generateSecret() {
+  DartRuntimeService._({
+    required this.config,
+    required DartRuntimeServiceBackendBuilder backendBuilder,
+  }) : authCode = config.disableAuthCodes ? null : generateSecret() {
     if (config.enableLogging) {
       _logger.onRecord.listen(stdout.writeln);
     }
+    backend = backendBuilder(this);
   }
 
   static Future<DartRuntimeService> initialize({
     required DartRuntimeServiceOptions config,
-    required DartRuntimeServiceBackend backend,
+    required DartRuntimeServiceBackendBuilder backendBuilder,
   }) async {
-    final service = DartRuntimeService._(config: config, backend: backend);
+    final service = DartRuntimeService._(
+      config: config,
+      backendBuilder: backendBuilder,
+    );
     await service._initialize();
     return service;
   }
 
   final DartRuntimeServiceOptions config;
 
-  final DartRuntimeServiceBackend backend;
+  late final DartRuntimeServiceBackend backend;
 
   /// The ws:// URI pointing to this [DartRuntimeService]'s server.
   ///
   /// Throws [DartRuntimeServiceServerNotRunning] if the HTTP server is not
   /// active.
+  ///
+  /// It's possible that the returned [Uri] is no longer valid if the server
+  /// was recently shut down.
   Uri get uri {
     if (_server == null) {
       throw const DartRuntimeServiceServerNotRunning();
@@ -58,6 +71,9 @@ class DartRuntimeService {
   ///
   /// Throws [DartRuntimeServiceServerNotRunning] if the HTTP server is not
   /// active.
+  ///
+  /// It's possible that the returned [Uri] is no longer valid if the server
+  /// was recently shut down.
   Uri get httpUri => uri.replace(scheme: 'http');
 
   /// The sse:// URI pointing to this [DartRuntimeService]'s server.
@@ -67,6 +83,9 @@ class DartRuntimeService {
   ///
   /// Throws [DartRuntimeServiceServerNotRunning] if the HTTP server is not
   /// active.
+  ///
+  /// It's possible that the returned [Uri] is no longer valid if the server
+  /// was recently shut down.
   Uri get sseUri {
     if (config.sseHandlerPath == null) {
       throw StateError('SSE handler path not configured.');
@@ -92,11 +111,16 @@ class DartRuntimeService {
 
   @visibleForTesting
   late final eventStreamManager = EventStreamManager(
+    backend: backend,
     clientsGetter: () => UnmodifiableNamedLookup(clientManager.clients),
   );
 
+  // TODO(bkonyi): this should be protected by a mutex.
   HttpServer? _server;
 
+  /// Returns true if the HTTP server is active.
+  bool get isServerRunning => _server != null;
+
   /// Initializes the service's state without starting the web server.
   Future<void> _initialize() async {
     await backend.initialize();
@@ -117,15 +141,46 @@ class DartRuntimeService {
     Logger.root.clearListeners();
   }
 
+  /// Enables or disables the server based on the value of [enable].
+  ///
+  /// [silenceOutput] is used to determine if the service will output
+  /// non-logging information to the terminal.
+  ///
+  /// This is called when `dart:developer`'s [Service.controlWebServer] is
+  /// invoked.
+  // TODO(bkonyi): respect silenceOutput
+  Future<void> serverControl({
+    required bool enable,
+    bool? silenceOutput,
+  }) async {
+    // TODO(bkonyi): verify there's no race conditions
+    if (!enable && isServerRunning) {
+      await _shutdownServer();
+    } else if (enable && !isServerRunning) {
+      await _startServer();
+    }
+  }
+
+  /// Toggles the state of the HTTP server, enabling it if it's not running and
+  /// disabling it if it is running.
   Future<void> toggleServer() async {
     // TODO(bkonyi): verify there's no race conditions
-    if (_server != null) {
+    if (isServerRunning) {
       await _shutdownServer();
     } else {
       await _startServer();
     }
   }
 
+  /// Creates an artificial client to process JSON-RPC requests from
+  /// non-standard sources (e.g., from native code).
+  void addArtificialClient({
+    required StreamChannel<String> connection,
+    required String name,
+  }) {
+    clientManager.addClient(connection: connection, name: name);
+  }
+
   Future<void> _startServer() async {
     if (_server != null) {
       _logger.warning(
@@ -193,6 +248,11 @@ class DartRuntimeService {
     await server.close();
   }
 
+  /// Send a [StreamEvent] to subscribed clients.
+  void sendEvent({required StreamEvent event}) {
+    event.send(eventStreamMethods: eventStreamManager);
+  }
+
   shelf.Handler _handlers() {
     _logger.info('Building Shelf handlers.');
     var pipeline = const shelf.Pipeline();
diff --git a/pkg/dart_runtime_service/lib/src/dart_runtime_service_backend.dart b/pkg/dart_runtime_service/lib/src/dart_runtime_service_backend.dart
index fc814d307ba..29d3c94efc3 100644
--- a/pkg/dart_runtime_service/lib/src/dart_runtime_service_backend.dart
+++ b/pkg/dart_runtime_service/lib/src/dart_runtime_service_backend.dart
@@ -3,16 +3,28 @@
 // BSD-style license that can be found in the LICENSE file.
 
 import 'package:json_rpc_2/json_rpc_2.dart' as json_rpc;
+import 'package:meta/meta.dart';
 
 import 'dart_runtime_service.dart';
+import 'event_streams.dart';
+import 'isolate_manager.dart';
 
 /// A backend implementation of a service used to inject non-common
 /// functionality into a [DartRuntimeService].
-abstract class DartRuntimeServiceBackend {
+abstract class DartRuntimeServiceBackend<IM extends IsolateManager> {
+  DartRuntimeServiceBackend({required this.frontend});
+
+  /// The active service frontend hosting this [DartRuntimeServiceBackend].
+  final DartRuntimeService frontend;
+
+  /// Manages and tracks the lifecycle of isolates for the backend.
+  IM get isolateManager;
+
   /// Invoked by the [DartRuntimeService] when the service is initializing,
   /// before the service's HTTP server is started.
   ///
   /// The backend should not expect for this to be invoked more than once.
+  @mustCallSuper
   Future<void> initialize();
 
   /// Invoked by the [DartRuntimeService] once it has completely finished
@@ -38,6 +50,24 @@ abstract class DartRuntimeServiceBackend {
   /// started.
   Future<void> onServerStarted({required Uri httpUri, required Uri wsUri});
 
+  /// Invoked when [EventStreamManager.streamListen] is called and the first
+  /// client has subscribed to [streamId].
+  ///
+  /// [params] contains all of the parameters sent as part of the
+  /// `streamListen` request.
+  ///
+  /// Returns true when the stream was successfully listened to.
+  bool onStreamListen({
+    required String streamId,
+    required Map<String, Object?> params,
+  }) {
+    return true;
+  }
+
+  /// Invoked when [EventStreamManager.streamCancel] is called and there are no
+  /// more clients listening to [streamId].
+  void onStreamCancel({required String streamId}) {}
+
   /// Invoked by the [DartRuntimeService] to register handlers for the RPCs
   /// provided by the backend.
   void registerRpcs(json_rpc.Peer clientPeer);
diff --git a/pkg/dart_runtime_service/lib/src/dart_runtime_service_rpcs.dart b/pkg/dart_runtime_service/lib/src/dart_runtime_service_rpcs.dart
index ff9066cc517..91e1dde9182 100644
--- a/pkg/dart_runtime_service/lib/src/dart_runtime_service_rpcs.dart
+++ b/pkg/dart_runtime_service/lib/src/dart_runtime_service_rpcs.dart
@@ -201,9 +201,13 @@ final class DartRuntimeServiceRpcs {
   ///
   /// If the stream ID does not correspond with a known stream, an error
   /// response may be returned.
-  RpcResponse streamListen(json_rpc.Parameters parameters) {
+  Future<RpcResponse> streamListen(json_rpc.Parameters parameters) async {
     final stream = parameters[_kStreamId].asString;
-    eventStreamMethods.streamListen(client: client, streamId: stream);
+    eventStreamMethods.streamListen(
+      client: client,
+      streamId: stream,
+      params: parameters.asMap.cast<String, Object?>(),
+    );
     return Success().toJson();
   }
 
@@ -214,7 +218,7 @@ final class DartRuntimeServiceRpcs {
   ///
   /// If the stream ID does not correspond with a known stream, an error
   /// response may be returned.
-  RpcResponse streamCancel(json_rpc.Parameters parameters) {
+  Future<RpcResponse> streamCancel(json_rpc.Parameters parameters) async {
     final streamId = parameters[_kStreamId].asString;
     eventStreamMethods.streamCancel(client: client, streamId: streamId);
     return Success().toJson();
diff --git a/pkg/dart_runtime_service/lib/src/event_streams.dart b/pkg/dart_runtime_service/lib/src/event_streams.dart
index 80975f23d9b..1eec13bf733 100644
--- a/pkg/dart_runtime_service/lib/src/event_streams.dart
+++ b/pkg/dart_runtime_service/lib/src/event_streams.dart
@@ -10,6 +10,7 @@ import 'package:meta/meta.dart';
 import 'package:vm_service/vm_service.dart';
 
 import 'clients.dart';
+import 'dart_runtime_service_backend.dart';
 import 'rpc_exceptions.dart';
 import 'utils.dart';
 
@@ -109,8 +110,16 @@ abstract interface class EventStreamMethods {
     ServiceAlias alias,
   );
 
-  /// Subscribes `client` to a stream.
-  void streamListen({required Client client, required String streamId});
+  /// Subscribes [client] to a stream.
+  ///
+  /// [params] is the unaltered set of parameters included when `streamListen`
+  /// is invoked. Backends may use these additional parameters for special
+  /// behavior (e.g., changing the verbosity of responses).
+  void streamListen({
+    required Client client,
+    required String streamId,
+    required Map<String, Object?> params,
+  });
 
   /// Unsubscribes `client` from a stream.
   void streamCancel({required Client client, required String streamId});
@@ -122,13 +131,12 @@ abstract interface class EventStreamMethods {
 /// Used for keeping track of stream subscription state and sending events to
 /// clients subscribed to individual streams.
 class EventStreamManager implements EventStreamMethods {
-  EventStreamManager({
-    required UnmodifiableNamedLookup<Client> Function() clientsGetter,
-  }) : _clientsGetter = clientsGetter;
+  EventStreamManager({required this._clientsGetter, required this._backend});
 
   static const kStreamNotify = 'streamNotify';
 
   final UnmodifiableNamedLookup<Client> Function() _clientsGetter;
+  final DartRuntimeServiceBackend _backend;
   late final clients = _clientsGetter();
 
   @visibleForTesting
@@ -225,14 +233,23 @@ class EventStreamManager implements EventStreamMethods {
 
   /// Subscribes `client` to a stream.
   @override
-  void streamListen({required Client client, required String streamId}) {
+  void streamListen({
+    required Client client,
+    required String streamId,
+    required Map<String, Object?> params,
+  }) {
     assert(streamId.isNotEmpty);
-    // TODO(bkonyi): invoke backend stream handling logic.
     final listeners = streamListeners.putIfAbsent(streamId, () => []);
     if (listeners.contains(client)) {
       RpcException.streamAlreadySubscribed.throwException();
     }
     listeners.add(client);
+
+    // Tell the backend to start sending events for this stream if this is the
+    // first listener.
+    if (listeners.length == 1) {
+      _backend.onStreamListen(streamId: streamId, params: params);
+    }
     if (streamId == EventStreams.kService) {
       // Send all previously registered service extensions when a client
       // subscribes to the Service stream.
@@ -265,7 +282,11 @@ class EventStreamManager implements EventStreamMethods {
     }
 
     listeners.remove(client);
-    // TODO(bkonyi): invoke backend stream handling logic.
+    // Tell the backend to stop sending events for this stream if there's no
+    // more listeners.
+    if (listeners.isEmpty) {
+      _backend.onStreamCancel(streamId: streamId);
+    }
   }
 
   /// Cleanup stream subscriptions for `client` when it has disconnected.
diff --git a/pkg/dart_runtime_service/lib/src/handlers.dart b/pkg/dart_runtime_service/lib/src/handlers.dart
index 46ab0553e19..a3aae226053 100644
--- a/pkg/dart_runtime_service/lib/src/handlers.dart
+++ b/pkg/dart_runtime_service/lib/src/handlers.dart
@@ -61,7 +61,7 @@ Handler webSocketClientHandler({required ClientManager clientManager}) =>
       // package:shelf_web_socket v2.
       final logger = Logger('WebSocketHandler');
       logger.info('New web socket connection. Creating $Client.');
-      clientManager.addClient(ws.cast<String>());
+      clientManager.addClient(connection: ws.cast<String>());
     });
 
 /// Creates a [Handler] for incoming SSE connections.
@@ -82,7 +82,7 @@ Handler sseClientHandler({
 
   handler.connections.rest.listen((sseConnection) {
     logger.info('New SSE connection. Creating $Client.');
-    clientManager.addClient(sseConnection);
+    clientManager.addClient(connection: sseConnection);
   });
 
   return handler.handler;
diff --git a/pkg/dart_runtime_service/lib/src/isolate_manager.dart b/pkg/dart_runtime_service/lib/src/isolate_manager.dart
new file mode 100644
index 00000000000..5208dd63b6a
--- /dev/null
+++ b/pkg/dart_runtime_service/lib/src/isolate_manager.dart
@@ -0,0 +1,178 @@
+// Copyright (c) 2026, the Dart project authors.  Please see the AUTHORS file
+// for details. All rights reserved. Use of this source code is governed by a
+// BSD-style license that can be found in the LICENSE file.
+
+import 'dart:async';
+
+import 'package:json_rpc_2/error_code.dart' as json_rpc_error;
+import 'package:json_rpc_2/json_rpc_2.dart' as json_rpc;
+import 'package:logging/logging.dart';
+import 'package:meta/meta.dart';
+
+import 'dart_runtime_service.dart';
+
+enum IsolateState {
+  start,
+  running,
+  pauseStart,
+  pauseExit,
+  pausePostRequest,
+  unknown,
+}
+
+/// Base class for representing the state of a running isolate.
+base class RunningIsolate {
+  RunningIsolate({required this.id, required this.name})
+    : _state = IsolateState.unknown;
+
+  late final _logger = Logger('Isolate ($name)');
+  final String name;
+  final int id;
+  // ignore: unused_field, will be used for resume permission logic.
+  IsolateState _state;
+
+  /// Invoked when the isolate has shutdown.
+  ///
+  /// Override this to clean up any state associated with this isolate.
+  @mustCallSuper
+  void shutdown() {
+    _logger.info('Shutting down.');
+  }
+
+  // State setters.
+  void pausedOnExit() => _stateChange(IsolateState.pauseExit);
+
+  void pausedOnStart() => _stateChange(IsolateState.pauseStart);
+
+  void pausedPostRequest() => _stateChange(IsolateState.pausePostRequest);
+
+  void resumed() => running();
+
+  void running() => _stateChange(IsolateState.running);
+
+  void started() => _stateChange(IsolateState.start);
+
+  void _stateChange(IsolateState updated) {
+    _logger.info('${_state.name} => ${updated.name}');
+    _state = updated;
+  }
+
+  @override
+  String toString() => 'Isolate(name: $name id: $id)';
+}
+
+/// This file contains functionality used to track the running state of
+/// all isolates in a given Dart process.
+///
+/// [RunningIsolate] is a representation of a single live isolate and contains
+/// running state information for that isolate. In addition, approvals from
+/// clients used to synchronize isolate resuming across multiple clients are
+/// tracked in this class.
+///
+/// The [IsolateManager] keeps track of all the isolates in the
+/// target process and handles isolate lifecycle events including:
+///   - Startup
+///   - Shutdown
+///   - Pauses
+///
+/// The [IsolateManager] also handles the `resume` RPC, which checks the
+/// resume approvals in the target [RunningIsolate] to determine if the
+/// isolate should be resumed or wait for additional approvals to be granted.
+abstract base class IsolateManager {
+  final _logger = Logger('$IsolateManager');
+  final isolates = <int, RunningIsolate>{};
+
+  /// The ID of the root isolate.
+  ///
+  /// Used to support the `isolates/root` isolate ID.
+  int? _rootIsolateId;
+
+  @mustCallSuper
+  Future<void> shutdown() async {
+    _logger.info('Shutting down.');
+  }
+
+  /// Forwards the RPC request for [method] to be handled in the context of an
+  /// isolate.
+  ///
+  /// [params] is the set of parameters for the RPC and must include a valid
+  /// `isolateId`.
+  Future<RpcResponse> sendToIsolate({
+    required String method,
+    required Map<String, Object?> params,
+  });
+
+  /// Initializes state for a newly started isolate.
+  void isolateStarted({required RunningIsolate isolate}) {
+    _logger.info('Starting isolate: $isolate');
+    if (_rootIsolateId == null) {
+      // TODO(bkonyi): ensure this is a non-system isolate
+      _logger.info('$isolate is the root isolate.');
+      _rootIsolateId = isolate.id;
+    }
+    isolate.running();
+    isolates[isolate.id] = isolate;
+  }
+
+  /// Cleans up state for an isolate that has exited.
+  void isolateExited({required int id}) {
+    final isolate = isolates.remove(id);
+    if (isolate == null) {
+      _logger.warning(
+        'isolateExited called with id: $id, but the isolate is not registered. '
+        'Ignoring.',
+      );
+      return;
+    }
+    _logger.info('Isolate exited: $isolate');
+    isolate.shutdown();
+  }
+
+  /// Looks up a [RunningIsolate] based on the `isolateId` entry in [params].
+  ///
+  /// If the isolate ID is malformed, a [json_rpc.RpcException] is thrown with
+  /// an invalid parameters error.
+  ///
+  /// If the isolate ID is not associated with a running isolate, null is
+  /// returned.
+  RunningIsolate? lookupIsolateFromParams({
+    required String method,
+    required Map<String, Object?> params,
+  }) {
+    const kIsolateId = 'isolateId';
+    const kIsolateIdPrefix = 'isolates/';
+    assert(params.containsKey(kIsolateId));
+    final isolateIdParam = params[kIsolateId] as String;
+
+    Never throwInvalidIsolateId() => throw json_rpc.RpcException(
+      json_rpc_error.INVALID_PARAMS,
+      'Invalid params',
+      data: {
+        'details':
+            "$method: invalid '$kIsolateId' parameter: "
+            '$isolateIdParam',
+      },
+    );
+
+    if (!isolateIdParam.startsWith(kIsolateIdPrefix)) {
+      _logger.warning('Malformed $kIsolateId: $isolateIdParam');
+      throwInvalidIsolateId();
+    }
+
+    final isolateId = isolateIdParam.substring(kIsolateIdPrefix.length);
+    int id;
+    if (isolateId == 'root') {
+      if (_rootIsolateId == null) {
+        throwInvalidIsolateId();
+      }
+      id = _rootIsolateId!;
+    } else {
+      try {
+        id = int.parse(isolateId);
+      } on FormatException {
+        throwInvalidIsolateId();
+      }
+    }
+    return isolates[id];
+  }
+}
diff --git a/pkg/dart_runtime_service/lib/src/rpc_exceptions.dart b/pkg/dart_runtime_service/lib/src/rpc_exceptions.dart
index 05252cbae07..9693dea9b16 100644
--- a/pkg/dart_runtime_service/lib/src/rpc_exceptions.dart
+++ b/pkg/dart_runtime_service/lib/src/rpc_exceptions.dart
@@ -21,7 +21,11 @@ enum RpcException {
   const RpcException({required this.code, required this.message});
 
   /// Throws a [json_rpc.RpcException] with [code] and [message].
-  Never throwException() => throw json_rpc.RpcException(code, message);
+  Never throwException() => throw toException();
+
+  /// Builds a [json_rpc.RpcException] with [code] and [message] without
+  /// throwing.
+  json_rpc.RpcException toException() => json_rpc.RpcException(code, message);
 
   /// The JSON-RPC error code.
   final int code;
diff --git a/pkg/dart_runtime_service/pubspec.yaml b/pkg/dart_runtime_service/pubspec.yaml
index bf57ca029b7..e0ed77ed3b8 100644
--- a/pkg/dart_runtime_service/pubspec.yaml
+++ b/pkg/dart_runtime_service/pubspec.yaml
@@ -3,7 +3,7 @@ name: dart_runtime_service
 publish_to: none
 
 environment:
-  sdk: ^3.8.0
+  sdk: ^3.12.0-edge
 
 resolution: workspace
 
diff --git a/pkg/dart_runtime_service/test/utils/mocks.dart b/pkg/dart_runtime_service/test/utils/mocks.dart
index b55dc26ebc2..4c5df770ca8 100644
--- a/pkg/dart_runtime_service/test/utils/mocks.dart
+++ b/pkg/dart_runtime_service/test/utils/mocks.dart
@@ -36,4 +36,21 @@ base class FakeDartRuntimeServiceBackend extends Fake
 
   @override
   void registerFallbacks(json_rpc.Peer clientPeer) {}
+
+  @override
+  DartRuntimeService get frontend => throw UnimplementedError();
+
+  @override
+  IsolateManager get isolateManager => throw UnimplementedError();
+
+  @override
+  void onStreamCancel({required String streamId}) {}
+
+  @override
+  bool onStreamListen({
+    required String streamId,
+    required Map<String, Object?> params,
+  }) {
+    return true;
+  }
 }
diff --git a/pkg/dart_runtime_service/test/utils/utilities.dart b/pkg/dart_runtime_service/test/utils/utilities.dart
index 7f25c231fc9..6c2a2cd0df0 100644
--- a/pkg/dart_runtime_service/test/utils/utilities.dart
+++ b/pkg/dart_runtime_service/test/utils/utilities.dart
@@ -24,7 +24,7 @@ Future<DartRuntimeService> createDartRuntimeServiceForTest({
 
   service = await DartRuntimeService.initialize(
     config: config,
-    backend: FakeDartRuntimeServiceBackend(),
+    backendBuilder: (_) => FakeDartRuntimeServiceBackend(),
   );
   return service;
 }
diff --git a/pkg/dart_runtime_service_vm/bin/vm_service_entrypoint.dart b/pkg/dart_runtime_service_vm/bin/vm_service_entrypoint.dart
index 2afe4c906a1..4ee611d44bc 100644
--- a/pkg/dart_runtime_service_vm/bin/vm_service_entrypoint.dart
+++ b/pkg/dart_runtime_service_vm/bin/vm_service_entrypoint.dart
@@ -4,9 +4,11 @@
 
 import 'dart:async';
 import 'dart:io';
+import 'dart:isolate';
 
 import 'package:dart_runtime_service/dart_runtime_service.dart';
 import 'package:dart_runtime_service_vm/dart_runtime_service_vm.dart';
+import 'package:dart_runtime_service_vm/src/vm_isolate_manager.dart';
 
 // ignore: unreachable_from_main
 const entrypoint = pragma(
@@ -63,6 +65,19 @@ bool _isFuchsia = false;
 Stream<ProcessSignal> Function(ProcessSignal signal)? _signalWatch;
 
 @entrypoint
+RawReceivePort boot() => DartRuntimeServiceVMBackend.isolateControlPort;
+
+final _isolateRegistrationStreamController = StreamController<VmRunningIsolate>(
+  sync: true,
+);
+
+@entrypoint
+// ignore: unused_element
+void _registerIsolate(int portId, SendPort sendPort, String name) =>
+    _isolateRegistrationStreamController.sink.add(
+      VmRunningIsolate(id: portId, name: name, sendPort: sendPort),
+    );
+
 // ignore: unused_element
 StreamSubscription<ProcessSignal>? _signalSubscription;
 
@@ -108,6 +123,10 @@ Future<void> main([List<String> args = const []]) async {
       disableAuthCodes: _authCodesDisabled,
       autoStart: _autoStart,
     ),
-    backend: DartRuntimeServiceVMBackend(signalWatch: _signalWatch!),
+    backendBuilder: (frontend) => DartRuntimeServiceVMBackend(
+      frontend: frontend,
+      signalWatch: _signalWatch!,
+      runningIsolatesStream: _isolateRegistrationStreamController.stream,
+    ),
   );
 }
diff --git a/pkg/dart_runtime_service_vm/lib/dart_runtime_service_vm.dart b/pkg/dart_runtime_service_vm/lib/dart_runtime_service_vm.dart
index 0404404818f..15d26fcbb2b 100644
--- a/pkg/dart_runtime_service_vm/lib/dart_runtime_service_vm.dart
+++ b/pkg/dart_runtime_service_vm/lib/dart_runtime_service_vm.dart
@@ -3,36 +3,99 @@
 // BSD-style license that can be found in the LICENSE file.
 
 import 'dart:async';
+import 'dart:convert';
 import 'dart:io';
+import 'dart:isolate';
 
 import 'package:dart_runtime_service/dart_runtime_service.dart';
 
 import 'package:json_rpc_2/json_rpc_2.dart' as json_rpc;
 import 'package:logging/logging.dart';
+import 'package:stream_channel/stream_channel.dart';
 
 import 'src/native_bindings.dart';
+import 'src/vm_isolate_manager.dart';
 
-class DartRuntimeServiceVMBackend extends DartRuntimeServiceBackend {
+class DartRuntimeServiceVMBackend
+    extends DartRuntimeServiceBackend<VmIsolateManager> {
   /// The backend implementation for the Dart VM Service.
   ///
   /// [signalWatch] is the internal implementation of [ProcessSignal.watch],
   /// which bypasses checks that prevent [ProcessSignal.sigquit] from being
   /// watched.
-  DartRuntimeServiceVMBackend({required this.signalWatch});
+  DartRuntimeServiceVMBackend({
+    required super.frontend,
+    required this.signalWatch,
+    required Stream<VmRunningIsolate> runningIsolatesStream,
+  }) : isolateManager = VmIsolateManager(
+         runningIsolatesStream: runningIsolatesStream,
+       );
+
+  static const int _kServiceExitMessageId = 0;
+  static const int _kIsolateStartupMessageId = 1;
+  static const int _kIsolateShutdownMessageId = 2;
+  static const int _kWebServerControlMessageId = 3;
+  static const int _kServerInfoMessageId = 4;
+
+  /// Signals an RPC coming from native code (instead of from a websocket
+  /// connection).  These calls are limited to simple request-response and do
+  /// not allow arbitrary json-rpc messages.
+  ///
+  /// The messages are an array of length 3:
+  ///   (kMethodCallFromNative, String jsonRequest, PortId replyPort).
+  static const int _kMethodCallFromNativeId = 5;
 
   /// The internal implementation of [ProcessSignal.watch].
   final Stream<ProcessSignal> Function(ProcessSignal signal) signalWatch;
+  StreamSubscription<ProcessSignal>? _sigquitSubscription;
+
+  /// The port the VM uses to send messages to the VM service.
+  static final isolateControlPort = RawReceivePort();
+
+  /// Used to create an artificial client from within the VM service, allowing
+  /// for VM service requests to be made from within the VM or through the Dart
+  /// embedding API.
+  final _nativeRpcClientStreamChannelController =
+      StreamChannelController<String>(sync: true);
+
+  /// Iterator for RPC responses sent to the artificial client.
+  late final _nativeRpcClientResponseStream = StreamIterator(
+    _nativeRpcClientStreamChannelController.local.stream,
+  );
 
   final _nativeBindings = NativeBindings();
-  final _logger = Logger('VM Backend');
+  final _logger = Logger('$DartRuntimeServiceVMBackend');
 
-  StreamSubscription<ProcessSignal>? _sigquitSubscription;
+  @override
+  final VmIsolateManager isolateManager;
 
   @override
   Future<void> initialize() async {
     _logger.info('Initializing...');
+    isolateControlPort.handler = _vmMessageHandler;
+    frontend.addArtificialClient(
+      name: 'native-rpc-client',
+      connection: _nativeRpcClientStreamChannelController.foreign,
+    );
     _nativeBindings.onStart();
-    _logger.info('Initialized!');
+    _logger.info('Initialized.');
+  }
+
+  @override
+  Future<void> clearState() async {
+    // Do nothing for now.
+  }
+
+  @override
+  Future<void> shutdown() async {
+    _logger.info('Shutting down...');
+    await Future.wait([
+      _sigquitSubscription?.cancel() ?? Future<void>.value(),
+      _nativeRpcClientStreamChannelController.local.sink.close(),
+    ]);
+    isolateControlPort.close();
+    _nativeBindings.onExit();
+    _logger.info('Shutdown.');
   }
 
   @override
@@ -53,19 +116,28 @@ class DartRuntimeServiceVMBackend extends DartRuntimeServiceBackend {
     required Uri wsUri,
   }) async {
     // TODO(bkonyi): handle DDS connection case.
-    stdout.writeln('The Dart VM service is listening on $httpUri');
+    stdout.writeln('The Dart VM service is listening on $httpUri/');
     _nativeBindings.onServerAddressChange(httpUri.toString());
   }
 
   @override
-  Future<void> clearState() async {
-    // Do nothing for now.
+  bool onStreamListen({
+    required String streamId,
+    required Map<String, Object?> params,
+  }) {
+    var includePrivates = false;
+    if (params case {'includePrivates': final bool value}) {
+      includePrivates = value;
+    }
+    return _nativeBindings.streamListen(
+      streamId: streamId,
+      includePrivates: includePrivates,
+    );
   }
 
   @override
-  Future<void> shutdown() async {
-    await _sigquitSubscription?.cancel();
-    _nativeBindings.onExit();
+  void onStreamCancel({required String streamId}) {
+    _nativeBindings.streamCancel(streamId: streamId);
   }
 
   @override
@@ -85,9 +157,168 @@ class DartRuntimeServiceVMBackend extends DartRuntimeServiceBackend {
     final method = request.method;
     final params = request.asMap.cast<String, Object?>();
     if (params case {'isolateId': final String _}) {
-      // TODO(bkonyi): handle isolate requests
-      RpcException.serverError.throwException();
+      _logger.info(
+        'Sending request to isolate. Method: $method Params: $params',
+      );
+      return await isolateManager.sendToIsolate(method: method, params: params);
     }
+    _logger.info('Sending request to VM. Method: $method Params: $params');
     return await _nativeBindings.sendToVM(method: method, params: params);
   }
+
+  /// Handles messages sent directly from the VM via the isolate control port.
+  ///
+  /// Messages sent over the isolate control port include:
+  ///   - Stream events
+  ///   - Request to shutdown the service
+  ///   - RPC invocations from the VM or VM's embedder
+  ///   - dart:developer API invocations (e.g. Service.getInfo() and
+  ///     Service.toggleWebServer())
+  ///   - Isolate startup and shutdown notifications
+  void _vmMessageHandler(List<Object?> message) {
+    _logger.info('VM message: $message');
+    switch (message) {
+      case [final String streamId, final String eventJsonString]:
+        // This is an event.
+        _eventMessageHandler(
+          streamId,
+          json.decode(eventJsonString) as Map<String, Object?>,
+        );
+      case [final int opcode]:
+        // This is a control message directing the vm service to exit.
+        assert(opcode == _kServiceExitMessageId);
+        frontend.shutdown();
+      case [
+            final int opcode,
+            final List<int> messageBytes,
+            final SendPort replyPort,
+          ]
+          when opcode == _kMethodCallFromNativeId:
+        _handleNativeRpcCall(messageBytes, replyPort);
+      case [
+            final int opcode,
+            final SendPort sendPort,
+            final bool enable,
+            final bool? silenceOutput,
+          ]
+          when opcode == _kWebServerControlMessageId ||
+              opcode == _kServerInfoMessageId:
+        // This is a message interacting with the web server.
+        _serverMessageHandler(opcode, sendPort, enable, silenceOutput);
+      case [
+            final int opcode,
+            final int portId,
+            final SendPort sendPort,
+            final String name,
+          ]
+          when opcode == _kIsolateStartupMessageId ||
+              opcode == _kIsolateShutdownMessageId:
+        // This is a message informing us of the birth or death of an
+        // isolate.
+        _isolateControlMessageHandler(opcode, portId, sendPort, name);
+      default:
+        print('Internal vm-service error: ignoring illegal message: $message');
+    }
+  }
+
+  /// Forward VM service events sent from the VM.
+  void _eventMessageHandler(String streamId, Map<String, Object?> event) {
+    frontend.sendEvent(
+      event: ForwardingStreamEvent(streamId: streamId, event: event),
+    );
+  }
+
+  /// Handle notifications from the VM related to isolate startup and shutdown.
+  void _isolateControlMessageHandler(
+    int code,
+    int portId,
+    SendPort sp,
+    String name,
+  ) {
+    switch (code) {
+      case _kIsolateStartupMessageId:
+        isolateManager.onIsolateStartupMessage(
+          id: portId,
+          sendPort: sp,
+          name: name,
+        );
+      case _kIsolateShutdownMessageId:
+        isolateManager.onIsolateShutdownMessage(id: portId);
+    }
+  }
+
+  /// Handle requests from the VM related to the state of the service's HTTP
+  /// server.
+  Future<void> _serverMessageHandler(
+    int code,
+    SendPort sp,
+    bool enable,
+    bool? silenceOutput,
+  ) async {
+    void sendServerInfo() {
+      try {
+        sp.send(frontend.httpUri.toString());
+      } on DartRuntimeServiceServerNotRunning {
+        sp.send(null);
+      }
+    }
+
+    switch (code) {
+      case _kWebServerControlMessageId:
+        await frontend.serverControl(
+          enable: enable,
+          silenceOutput: silenceOutput,
+        );
+        sendServerInfo();
+      case _kServerInfoMessageId:
+        sendServerInfo();
+    }
+  }
+
+  /// Handle VM service requests from native code (see
+  /// `Dart_InvokeVMServiceMethod` in `dart_tools_api.h`).
+  Future<void> _handleNativeRpcCall(
+    List<int> message,
+    SendPort replyPort,
+  ) async {
+    final messageStr = utf8.decode(message);
+    _logger.info('Native RPC request: $messageStr');
+    _nativeRpcClientStreamChannelController.local.sink.add(messageStr);
+
+    // TODO(bkonyi): handle non-string results
+    /*
+    late List<int> bytes;
+    switch (response.kind) {
+      case ResponsePayloadKind.String:
+        bytes = utf8.encode(response.payload as String);
+        bytes = bytes is Uint8List ? bytes : Uint8List.fromList(bytes);
+      case ResponsePayloadKind.Binary:
+      case ResponsePayloadKind.Utf8String:
+        bytes = response.payload as Uint8List;
+    }
+    */
+
+    if (!await _nativeRpcClientResponseStream.moveNext()) {
+      _logger.warning('Native RPC client stream has closed.');
+      return;
+    }
+    _logger.info(
+      'Response received: ${_nativeRpcClientResponseStream.current}',
+    );
+    replyPort.send(utf8.encode(_nativeRpcClientResponseStream.current));
+  }
+}
+
+final class ForwardingStreamEvent extends StreamEvent {
+  ForwardingStreamEvent({required super.streamId, required this.event})
+    : super(kind: '<ignored>');
+
+  static const kParams = 'params';
+
+  Map<String, Object?> event;
+
+  @override
+  Map<String, Object?> toJson() {
+    return event[kParams] as Map<String, Object?>;
+  }
 }
diff --git a/pkg/dart_runtime_service_vm/lib/src/native_bindings.dart b/pkg/dart_runtime_service_vm/lib/src/native_bindings.dart
index ee400b34102..5bf667ffb82 100644
--- a/pkg/dart_runtime_service_vm/lib/src/native_bindings.dart
+++ b/pkg/dart_runtime_service_vm/lib/src/native_bindings.dart
@@ -16,11 +16,20 @@ import 'dart:typed_data';
 
 import 'package:dart_runtime_service/dart_runtime_service.dart';
 import 'package:json_rpc_2/json_rpc_2.dart' as json_rpc;
+import 'package:logging/logging.dart';
+
+import 'vm_isolate_manager.dart';
 
 /// Allows for sending messages to the native VM service implementation.
 class NativeBindings {
+  factory NativeBindings() => _instance;
+  NativeBindings._();
+
+  static final NativeBindings _instance = NativeBindings._();
   static final jsonUtf8Decoder = json.fuse(utf8);
 
+  final _logger = Logger('$NativeBindings');
+
   /// Sends a general RPC to the VM for processing.
   ///
   /// The RPC is not executed in the scope of any particular isolate.
@@ -44,6 +53,66 @@ class NativeBindings {
     return completer.future;
   }
 
+  /// Sends an RPC to a specific isolate for processing.
+  ///
+  /// The RPC is not executed in the scope of any particular isolate.
+  Future<RpcResponse> sendToIsolate({
+    required VmRunningIsolate isolate,
+    required String method,
+    required Map<String, Object?> params,
+  }) {
+    final receivePort = RawReceivePort(
+      null,
+      'Isolate Message (${isolate.name})',
+    );
+    // Keep track of receive port associated with the request so we can close
+    // it if isolate exits before sending a response.
+    isolate.outstandingRequestPorts.add(receivePort);
+    final completer = Completer<RpcResponse>();
+    receivePort.handler = (Object value) {
+      receivePort.close();
+      isolate.outstandingRequestPorts.remove(receivePort);
+      try {
+        completer.complete(_toResponse(value: value));
+      } on json_rpc.RpcException catch (e) {
+        completer.completeError(e);
+      }
+    };
+    if (!vm_service_natives.sendIsolateServiceMessage(
+      isolate.sendPort,
+      _toRequest(responsePort: receivePort, method: method, params: params),
+    )) {
+      receivePort.close();
+      isolate.outstandingRequestPorts.remove(receivePort);
+      _logger.warning('Could not send message to $isolate.');
+      completer.completeError(RpcException.internalError.toException());
+    }
+    return completer.future;
+  }
+
+  /// Notifies the VM to start sending events for [streamId].
+  ///
+  /// This only needs to be called once the first client has subscribed to the
+  /// stream. Subsequent subscriptions to the stream are handled by the
+  /// [EventStreamManager].
+  ///
+  /// If [includePrivates] is true, private event properties starting with '_'
+  /// will be included in events. This is false by default to reduce the size of
+  /// events for clients that don't rely on private properties.
+  bool streamListen({required String streamId, bool includePrivates = false}) =>
+      // TODO(bkonyi): handle case where some clients want privates included
+      // and others don't.
+      vm_service_natives.vmListenStream(streamId, includePrivates);
+
+  /// Notifies the VM to stop sending events for [streamId].
+  ///
+  /// This only needs to be called once the last client subscribed to the
+  /// stream has cancelled its subscription or disconnected. While clients have
+  /// active subscriptions to this stream, stream cancellation requests  are
+  /// handled by the [EventStreamManager].
+  void streamCancel({required String streamId}) =>
+      vm_service_natives.vmCancelStream(streamId);
+
   /// Notifies the VM that the VM service server has finished initializing.
   void onStart() => vm_service_natives.onStart();
 
diff --git a/pkg/dart_runtime_service_vm/lib/src/vm_isolate_manager.dart b/pkg/dart_runtime_service_vm/lib/src/vm_isolate_manager.dart
new file mode 100644
index 00000000000..094c944c57b
--- /dev/null
+++ b/pkg/dart_runtime_service_vm/lib/src/vm_isolate_manager.dart
@@ -0,0 +1,102 @@
+// Copyright (c) 2026, the Dart project authors. Please see the AUTHORS file
+// for details. All rights reserved. Use of this source code is governed by a
+// BSD-style license that can be found in the LICENSE file.
+
+import 'dart:async';
+import 'dart:isolate';
+
+import 'package:dart_runtime_service/dart_runtime_service.dart';
+import 'package:logging/logging.dart';
+import 'package:vm_service/vm_service.dart';
+
+import 'native_bindings.dart';
+
+/// A running isolate for the Dart VM.
+final class VmRunningIsolate extends RunningIsolate {
+  VmRunningIsolate({
+    required super.id,
+    required super.name,
+    required this.sendPort,
+  });
+
+  /// The port used to send service requests to the isolate within the VM.
+  final SendPort sendPort;
+
+  /// The set of ports for outstanding requests that are used by the VM to send
+  /// responses.
+  final outstandingRequestPorts = <RawReceivePort>{};
+
+  @override
+  void shutdown() {
+    for (final requestPort in outstandingRequestPorts) {
+      requestPort.close();
+    }
+    outstandingRequestPorts.clear();
+    super.shutdown();
+  }
+}
+
+/// Manages and tracks running isolates in the Dart VM.
+final class VmIsolateManager extends IsolateManager {
+  /// Initializes the [VmIsolateManager].
+  ///
+  /// [runningIsolatesStream] should be a stream of [VmRunningIsolate]s reported
+  /// by the Dart VM as started once the VM service has finished initializing.
+  VmIsolateManager({required Stream<VmRunningIsolate> runningIsolatesStream}) {
+    _runningIsolatesStreamSub = runningIsolatesStream.listen(
+      (isolate) => isolateStarted(isolate: isolate),
+    );
+  }
+
+  final _logger = Logger('$VmIsolateManager');
+  final _nativeBindings = NativeBindings();
+  late final StreamSubscription<VmRunningIsolate> _runningIsolatesStreamSub;
+
+  @override
+  Future<void> shutdown() async {
+    await _runningIsolatesStreamSub.cancel();
+    await super.shutdown();
+  }
+
+  /// Registers a newly started isolate reported via a message over the
+  /// service's control port.
+  void onIsolateStartupMessage({
+    required int id,
+    required SendPort sendPort,
+    required String name,
+  }) {
+    final isolate = VmRunningIsolate(id: id, name: name, sendPort: sendPort);
+    _logger.info('Isolate startup message received for $isolate');
+    isolateStarted(isolate: isolate);
+  }
+
+  /// Reports that an isolate is shutting down based on a message over the
+  /// service's control port.
+  void onIsolateShutdownMessage({required int id}) {
+    _logger.info('Isolate startup message received for isolate ID $id');
+    isolateExited(id: id);
+  }
+
+  @override
+  Future<RpcResponse> sendToIsolate({
+    required String method,
+    required Map<String, Object?> params,
+  }) async {
+    final isolate =
+        lookupIsolateFromParams(method: method, params: params)
+            as VmRunningIsolate?;
+    if (isolate == null) {
+      // There is some chance that this isolate may have lived before,
+      // so return a sentinel rather than an error.
+      return Sentinel(
+        kind: SentinelKind.kCollected,
+        valueAsString: '<collected>',
+      ).toJson();
+    }
+    return _nativeBindings.sendToIsolate(
+      isolate: isolate,
+      method: method,
+      params: params,
+    );
+  }
+}
diff --git a/pkg/dart_runtime_service_vm/pubspec.yaml b/pkg/dart_runtime_service_vm/pubspec.yaml
index 0f7be90657d..a2a044092d6 100644
--- a/pkg/dart_runtime_service_vm/pubspec.yaml
+++ b/pkg/dart_runtime_service_vm/pubspec.yaml
@@ -3,7 +3,7 @@ name: dart_runtime_service_vm
 publish_to: none
 
 environment:
-  sdk: ^3.8.0
+  sdk: ^3.12.0-edge
 
 resolution: workspace
 
@@ -12,3 +12,5 @@ dependencies:
   dart_runtime_service: any
   json_rpc_2: any
   logging: any
+  stream_channel: any
+  vm_service: any
diff --git a/runtime/bin/run_vm_tests.cc b/runtime/bin/run_vm_tests.cc
index 661267100ce..5bc2f56e823 100644
--- a/runtime/bin/run_vm_tests.cc
+++ b/runtime/bin/run_vm_tests.cc
@@ -110,8 +110,14 @@ static Dart_Isolate CreateAndSetupServiceIsolate(const char* script_uri,
   // vm/cc tests to randomly time out due to inability to shut service-isolate
   // down.
   // Issue(https://dartbug.com/37741):
-  if ((strcmp(run_filter, "DartAPI_InvokeVMServiceMethod") != 0) &&
-      (strcmp(run_filter, "DartAPI_InvokeVMServiceMethod_Loop") != 0)) {
+  const bool is_service_test =
+      (strcmp(run_filter, "DartAPI_InvokeVMServiceMethod") == 0) ||
+      (strcmp(run_filter, "DartAPI_InvokeVMServiceMethod_Loop") == 0);
+  const bool is_exp_service_test =
+      (strcmp(run_filter, "DartAPI_InvokeVMServiceMethod_Exp") == 0) ||
+      (strcmp(run_filter, "DartAPI_InvokeVMServiceMethod_Loop_Exp") == 0);
+
+  if (!is_service_test && !is_exp_service_test) {
     return nullptr;
   }
 
@@ -122,21 +128,50 @@ static Dart_Isolate CreateAndSetupServiceIsolate(const char* script_uri,
                                 packages_config, /*app_snapshot=*/nullptr,
                                 /*isolate_run_app_snapshot=*/false);
 
-  const uint8_t* kernel_buffer = nullptr;
-  intptr_t kernel_buffer_size = 0;
-
-  bin::dfe.Init();
-  bin::dfe.LoadPlatform(&kernel_buffer, &kernel_buffer_size);
-  RELEASE_ASSERT(kernel_buffer != nullptr);
-
   flags->load_vmservice_library = true;
   flags->is_service_isolate = true;
-  isolate_group_data->SetKernelBufferUnowned(
-      const_cast<uint8_t*>(kernel_buffer), kernel_buffer_size);
-  isolate = Dart_CreateIsolateGroupFromKernel(
-      script_uri, DART_VM_SERVICE_ISOLATE_NAME, kernel_buffer,
-      kernel_buffer_size, flags, isolate_group_data, /*isolate_data=*/nullptr,
-      error);
+
+#if defined(EXPERIMENTAL_VM_SERVICE)
+  if (is_exp_service_test) {
+    ASSERT(!is_service_test);
+    const uint8_t* isolate_snapshot_data = nullptr;
+    const uint8_t* isolate_snapshot_instructions = nullptr;
+
+    bin::VmService::enable_experimental_vm_service = true;
+    auto [app_snapshot, script_name] = bin::Snapshot::TryReadSDKSnapshot(
+        "dart_runtime_service_vm.dart.snapshot");
+    if (app_snapshot == nullptr) {
+      return nullptr;
+    }
+    const uint8_t* ignore_vm_snapshot_data;
+    const uint8_t* ignore_vm_snapshot_instructions;
+    app_snapshot->SetBuffers(
+        &ignore_vm_snapshot_data, &ignore_vm_snapshot_instructions,
+        &isolate_snapshot_data, &isolate_snapshot_instructions);
+    isolate = Dart_CreateIsolateGroup(
+        script_uri, DART_VM_SERVICE_ISOLATE_NAME, isolate_snapshot_data,
+        isolate_snapshot_instructions, flags, isolate_group_data,
+        /*isolate_data=*/nullptr, error);
+  }
+#endif  // defined(EXPERIMENTAL_VM_SERVICE)
+
+  if (is_service_test) {
+    ASSERT(!is_exp_service_test);
+    const uint8_t* kernel_buffer = nullptr;
+    intptr_t kernel_buffer_size = 0;
+
+    bin::dfe.Init();
+    bin::dfe.LoadPlatform(&kernel_buffer, &kernel_buffer_size);
+    RELEASE_ASSERT(kernel_buffer != nullptr);
+
+    isolate_group_data->SetKernelBufferUnowned(
+        const_cast<uint8_t*>(kernel_buffer), kernel_buffer_size);
+    isolate = Dart_CreateIsolateGroupFromKernel(
+        script_uri, DART_VM_SERVICE_ISOLATE_NAME, kernel_buffer,
+        kernel_buffer_size, flags, isolate_group_data, /*isolate_data=*/nullptr,
+        error);
+  }
+
   if (isolate == nullptr) {
     delete isolate_group_data;
     return nullptr;
diff --git a/runtime/vm/dart_api_impl_test.cc b/runtime/vm/dart_api_impl_test.cc
index 3eb7ae70c4a..2af17157851 100644
--- a/runtime/vm/dart_api_impl_test.cc
+++ b/runtime/vm/dart_api_impl_test.cc
@@ -10559,11 +10559,11 @@ TEST_CASE(DartAPI_InvokeImportedFunction) {
       "NoSuchMethodError: No top-level method 'getCurrentTag' declared.");
 }
 
-TEST_CASE(DartAPI_InvokeVMServiceMethod) {
+static void InvokeVMServiceMethodCommon() {
   char buffer[1024];
   Utils::SNPrint(buffer, sizeof(buffer),
                  R"({
-                  "jsonrpc": 2.0,
+                  "jsonrpc": "2.0",
                   "id": "foo",
                   "method": "getVM",
                   "params": { }
@@ -10618,6 +10618,16 @@ TEST_CASE(DartAPI_InvokeVMServiceMethod) {
   EXPECT(result == Dart_True());
 }
 
+TEST_CASE(DartAPI_InvokeVMServiceMethod) {
+  InvokeVMServiceMethodCommon();
+}
+
+#if defined(EXPERIMENTAL_VM_SERVICE)
+TEST_CASE(DartAPI_InvokeVMServiceMethod_Exp) {
+  InvokeVMServiceMethodCommon();
+}
+#endif  // defined(EXPERIMENTAL_VM_SERVICE)
+
 static Monitor* loop_test_lock = new Monitor();
 static bool loop_test_exit = false;
 static bool loop_reset_count = false;
@@ -10630,7 +10640,7 @@ static void InvokeServiceMessages(uword param) {
   char buffer[1024];
   Utils::SNPrint(buffer, sizeof(buffer),
                  R"({
-                  "jsonrpc": 2.0,
+                  "jsonrpc": "2.0",
                   "id": "foo",
                   "method": "getVM",
                   "params": { }
@@ -10661,7 +10671,7 @@ static void InvokeServiceMessages(uword param) {
   } while (count < 100);
 }
 
-TEST_CASE(DartAPI_InvokeVMServiceMethod_Loop) {
+static void InvokeVMServiceMethodLoopCommon() {
   {
     MonitorLocker ml(loop_test_lock);
     loop_test_exit = false;
@@ -10673,6 +10683,16 @@ TEST_CASE(DartAPI_InvokeVMServiceMethod_Loop) {
   }
   OSThread::Join(loop_test_join_id);
 }
+
+TEST_CASE(DartAPI_InvokeVMServiceMethod_Loop) {
+  InvokeVMServiceMethodLoopCommon();
+}
+
+#if defined(EXPERIMENTAL_VM_SERVICE)
+TEST_CASE(DartAPI_InvokeVMServiceMethod_Loop_Exp) {
+  InvokeVMServiceMethodLoopCommon();
+}
+#endif  // defined(EXPERIMENTAL_VM_SERVICE)
 #endif  // !defined(PRODUCT)
 
 static void HandleResponse(Dart_Port dest_port_id, Dart_CObject* message) {
diff --git a/runtime/vm/service_isolate.cc b/runtime/vm/service_isolate.cc
index b680bf8f559..fd6613600b8 100644
--- a/runtime/vm/service_isolate.cc
+++ b/runtime/vm/service_isolate.cc
@@ -578,12 +578,18 @@ void ServiceIsolate::Shutdown() {
 
 void ServiceIsolate::BootVmServiceLibrary() {
   Thread* thread = Thread::Current();
-  const Library& vmservice_library =
-      Library::Handle(Library::LookupLibrary(thread, Symbols::DartVMService()));
-  ASSERT(!vmservice_library.IsNull());
+  Library& lib =
+      Library::Handle(thread->isolate_group()->object_store()->root_library());
   const String& boot_function_name = String::Handle(String::New("boot"));
-  const Function& boot_function = Function::Handle(
-      vmservice_library.LookupFunctionAllowPrivate(boot_function_name));
+  Function& boot_function =
+      Function::Handle(lib.LookupFunctionAllowPrivate(boot_function_name));
+
+  if (boot_function.IsNull()) {
+    lib ^= Library::LookupLibrary(thread, Symbols::DartVMService());
+    ASSERT(!lib.IsNull());
+    boot_function ^= lib.LookupFunctionAllowPrivate(boot_function_name);
+  }
+
   ASSERT(!boot_function.IsNull());
   const Object& result = Object::Handle(
       DartEntry::InvokeFunction(boot_function, Object::empty_array()));
@@ -608,16 +614,18 @@ void ServiceIsolate::RegisterRunningIsolates(
   ASSERT(thread->isolate()->is_service_isolate());
 
   // Obtain "_registerIsolate" function to call.
-  const String& library_url = Symbols::DartVMService();
-  ASSERT(!library_url.IsNull());
-  const Library& library =
-      Library::Handle(zone, Library::LookupLibrary(thread, library_url));
-  ASSERT(!library.IsNull());
-  const String& function_name =
-      String::Handle(zone, String::New("_registerIsolate"));
-  ASSERT(!function_name.IsNull());
-  const Function& register_function_ =
-      Function::Handle(zone, library.LookupFunctionAllowPrivate(function_name));
+  Library& lib =
+      Library::Handle(thread->isolate_group()->object_store()->root_library());
+  const String& function_name = String::Handle(String::New("_registerIsolate"));
+  Function& register_function_ =
+      Function::Handle(lib.LookupFunctionAllowPrivate(function_name));
+
+  if (register_function_.IsNull()) {
+    lib ^= Library::LookupLibrary(thread, Symbols::DartVMService());
+    ASSERT(!lib.IsNull());
+    register_function_ ^= lib.LookupFunctionAllowPrivate(function_name);
+  }
+
   ASSERT(!register_function_.IsNull());
 
   Integer& port_int = Integer::Handle(zone);