diff --git a/runtime/bin/dartutils.h b/runtime/bin/dartutils.h
index 228779000fc..b414d731ca9 100644
--- a/runtime/bin/dartutils.h
+++ b/runtime/bin/dartutils.h
@@ -651,6 +651,20 @@ class ScopedBlockingCall {
   DISALLOW_COPY_AND_ASSIGN(ScopedBlockingCall);
 };
 
+// Remove once we remove the limitation on the number of running mutators.
+// https://github.com/dart-lang/sdk/issues/54687
+class LeaveIsolateScope {
+ public:
+  LeaveIsolateScope() : isolate_(Dart_CurrentIsolate()) { Dart_ExitIsolate(); }
+  ~LeaveIsolateScope() { Dart_EnterIsolate(isolate_); }
+
+ private:
+  Dart_Isolate isolate_;
+
+  DISALLOW_ALLOCATION();
+  DISALLOW_COPY_AND_ASSIGN(LeaveIsolateScope);
+};
+
 struct MagicNumberData {
   static constexpr intptr_t kMaxLength = 8;
 
diff --git a/runtime/bin/process.cc b/runtime/bin/process.cc
index 309f69014d1..f990e80e3ac 100644
--- a/runtime/bin/process.cc
+++ b/runtime/bin/process.cc
@@ -285,6 +285,8 @@ void FUNCTION_NAME(Process_Sleep)(Dart_NativeArguments args) {
   int64_t milliseconds = 0;
   // Ignore result if passing invalid argument and just set exit code to 0.
   DartUtils::GetInt64Value(Dart_GetNativeArgument(args, 0), &milliseconds);
+
+  LeaveIsolateScope leave_isolate;
   TimerUtils::Sleep(milliseconds);
 }
 
diff --git a/runtime/bin/process_linux.cc b/runtime/bin/process_linux.cc
index 5439d4ec8a6..64e74fcfab9 100644
--- a/runtime/bin/process_linux.cc
+++ b/runtime/bin/process_linux.cc
@@ -849,6 +849,8 @@ bool Process::Wait(intptr_t pid,
 
   int alive = 3;
   while (alive > 0) {
+    LeaveIsolateScope leave_isolate;
+
     // Blocking call waiting for events from the child process.
     if (TEMP_FAILURE_RETRY(poll(fds, alive, -1)) <= 0) {
       return CloseProcessBuffers(fds, alive);
diff --git a/runtime/bin/process_macos.cc b/runtime/bin/process_macos.cc
index 24300eeb3c7..d7eb45e4ae0 100644
--- a/runtime/bin/process_macos.cc
+++ b/runtime/bin/process_macos.cc
@@ -826,6 +826,8 @@ bool Process::Wait(intptr_t pid,
 
   int alive = 3;
   while (alive > 0) {
+    LeaveIsolateScope leave_isolate;
+
     // Blocking call waiting for events from the child process.
     if (TEMP_FAILURE_RETRY(poll(fds, alive, -1)) <= 0) {
       return CloseProcessBuffers(fds, alive);
diff --git a/runtime/bin/process_win.cc b/runtime/bin/process_win.cc
index 44b61e0412c..e9a353b36c3 100644
--- a/runtime/bin/process_win.cc
+++ b/runtime/bin/process_win.cc
@@ -828,6 +828,8 @@ bool Process::Wait(intptr_t pid,
   // Continue until all handles are closed.
   int alive = kHandles;
   while (alive > 0) {
+    LeaveIsolateScope leave_isolate;
+
     // Blocking call waiting for events from the child process.
     DWORD wait_result = WaitForMultipleObjects(alive, events, FALSE, INFINITE);
 
diff --git a/runtime/tests/vm/dart/isolates/many_isolates_blocked_at_process_run_sync_test.dart b/runtime/tests/vm/dart/isolates/many_isolates_blocked_at_process_run_sync_test.dart
new file mode 100644
index 00000000000..42d4d9aa5fa
--- /dev/null
+++ b/runtime/tests/vm/dart/isolates/many_isolates_blocked_at_process_run_sync_test.dart
@@ -0,0 +1,25 @@
+// Copyright (c) 2024, 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:isolate";
+import "dart:io";
+
+child(replyPort) {
+  replyPort.send(null);
+  Process.runSync("sleep", ["3600"]);
+}
+
+main() async {
+  var pending = 0;
+  var port;
+  port = new RawReceivePort((msg) {
+    pending--;
+    if (pending == 0) exit(0);
+  });
+
+  for (var i = 0; i < 20; i++) {
+    Isolate.spawn(child, port.sendPort);
+    pending++;
+  }
+}
diff --git a/runtime/tests/vm/dart/isolates/many_isolates_blocked_at_sleep_test.dart b/runtime/tests/vm/dart/isolates/many_isolates_blocked_at_sleep_test.dart
new file mode 100644
index 00000000000..d053d684868
--- /dev/null
+++ b/runtime/tests/vm/dart/isolates/many_isolates_blocked_at_sleep_test.dart
@@ -0,0 +1,25 @@
+// Copyright (c) 2024, 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:isolate";
+import "dart:io";
+
+child(replyPort) {
+  replyPort.send(null);
+  sleep(Duration(minutes: 60));
+}
+
+main() async {
+  var pending = 0;
+  var port;
+  port = new RawReceivePort((msg) {
+    pending--;
+    if (pending == 0) exit(0);
+  });
+
+  for (var i = 0; i < 20; i++) {
+    Isolate.spawn(child, port.sendPort);
+    pending++;
+  }
+}