diff --git a/runtime/tests/vm/dart/thread_local_test.dart b/runtime/tests/vm/dart/thread_local_test.dart
new file mode 100644
index 00000000000..d651af15ddc
--- /dev/null
+++ b/runtime/tests/vm/dart/thread_local_test.dart
@@ -0,0 +1,32 @@
+// Copyright (c) 2025, 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.
+
+// Tests ThreadLocal.
+//
+// VMOptions=--experimental-shared-data
+
+import 'dart:isolate';
+import 'dart:_vm' show ThreadLocal;
+
+import 'package:expect/expect.dart';
+import 'package:expect/async_helper.dart';
+
+@pragma('vm:shared')
+final ThreadLocal<String> threadLocal = ThreadLocal<String>();
+
+void main() async {
+  asyncStart();
+  // Make sure that threadLocal retains its value even if underlying
+  // dart::Thread gets reclaimed and recreated.
+  final results = await List.generate(
+    64,
+    (_) => Isolate.run(() async {
+      threadLocal.value = "ok";
+      await Future.delayed(const Duration(milliseconds: 10));
+      return threadLocal.hasValue ? threadLocal.value : "fail";
+    }),
+  ).wait;
+  Expect.listEquals(['ok'], results.toSet().toList());
+  asyncEnd();
+}
diff --git a/runtime/vm/app_snapshot.cc b/runtime/vm/app_snapshot.cc
index 9727b41e48a..fdc1d793eeb 100644
--- a/runtime/vm/app_snapshot.cc
+++ b/runtime/vm/app_snapshot.cc
@@ -7546,7 +7546,6 @@ class ProgramDeserializationRoots : public DeserializationRoots {
 
     if (Snapshot::IncludesCode(d->kind())) {
       d->thread()->InitVMConstants();
-      d->thread()->set_thread_locals(Array::empty_array());
     }
 
     auto object_store = isolate_group->object_store();
diff --git a/runtime/vm/dart.cc b/runtime/vm/dart.cc
index f5f6a4d11b2..fad9553493c 100644
--- a/runtime/vm/dart.cc
+++ b/runtime/vm/dart.cc
@@ -791,7 +791,6 @@ char* Dart::InitializeIsolateGroup(Thread* T,
       ICData::Init();
       StubCode::Init();
       T->InitVMConstants();
-      T->set_thread_locals(Array::empty_array());
       Symbols::Init(IG);
       Object::FinishInit(IG);
       Api::InitHandles();
@@ -857,6 +856,8 @@ ErrorPtr Dart::InitializeIsolate(Thread* T,
     I->field_table()->MarkReadyToUse();
   }
 
+  T->set_thread_locals(Object::empty_array());
+
   const auto& error =
       Error::Handle(Z, I->isolate_object_store()->PreallocateObjects());
   if (!error.IsNull()) {
diff --git a/runtime/vm/object_store.h b/runtime/vm/object_store.h
index 5a59b3aa33e..716ebee7723 100644
--- a/runtime/vm/object_store.h
+++ b/runtime/vm/object_store.h
@@ -225,6 +225,7 @@ class ObjectPointerVisitor;
 #define ISOLATE_OBJECT_STORE_FIELD_LIST(R_, RW)                                \
   R_(Array, dart_args_1)                                                       \
   R_(Array, dart_args_2)                                                       \
+  RW(Array, thread_locals)                                                     \
   R_(GrowableObjectArray, resume_capabilities)                                 \
   R_(GrowableObjectArray, exit_listeners)                                      \
   R_(GrowableObjectArray, error_listeners)
diff --git a/runtime/vm/thread.cc b/runtime/vm/thread.cc
index c93d3c3eb51..0621e147621 100644
--- a/runtime/vm/thread.cc
+++ b/runtime/vm/thread.cc
@@ -279,6 +279,9 @@ void Thread::set_default_tag(const UserTag& tag) {
 }
 
 void Thread::set_thread_locals(const Array& thread_locals) {
+  if (isolate_ != nullptr) {
+    isolate_->isolate_object_store()->set_thread_locals(thread_locals);
+  }
   thread_locals_ = thread_locals.ptr();
 }
 
@@ -436,10 +439,6 @@ void Thread::EnterIsolate(Isolate* isolate) {
                              /*bypass_safepoint=*/false);
     thread->SetupMutatorState();
     thread->SetupDartMutatorState(isolate);
-
-    if (Array::empty_array().ptr() != nullptr) {
-      thread->set_thread_locals(Array::empty_array());
-    }
   }
 
   isolate->scheduled_mutator_thread_ = thread;
@@ -1643,6 +1642,7 @@ void Thread::ResetMutatorState() {
 
 void Thread::SetupDartMutatorState(Isolate* isolate) {
   field_table_values_ = isolate->field_table_->table();
+  thread_locals_ = isolate->isolate_object_store()->thread_locals();
 
   SetupDartMutatorStateDependingOnSnapshot(isolate->group());
 }
@@ -1682,6 +1682,7 @@ void Thread::ResetDartMutatorState() {
 
   field_table_values_ = nullptr;
   shared_field_table_values_ = nullptr;
+  thread_locals_ = Array::null();
   ONLY_IN_PRECOMPILED(global_object_pool_ = ObjectPool::null());
   ONLY_IN_PRECOMPILED(dispatch_table_array_ = nullptr);
 }
diff --git a/runtime/vm/thread_registry.cc b/runtime/vm/thread_registry.cc
index 9995b2a6c2c..b98474f0554 100644
--- a/runtime/vm/thread_registry.cc
+++ b/runtime/vm/thread_registry.cc
@@ -178,6 +178,7 @@ void ThreadRegistry::ReturnToFreelistLocked(Thread* thread) {
   ASSERT(thread->isolate_group_ == nullptr);
   ASSERT(thread->field_table_values_ == nullptr);
   ASSERT(thread->shared_field_table_values_ == nullptr);
+  ASSERT(thread->thread_locals_ == Array::null());
   ASSERT(threads_lock()->IsOwnedByCurrentThread());
   // Add thread to the free list.
   thread->next_ = free_list_;