diff --git a/doc/api/vm.md b/doc/api/vm.md
index 14cd1f269b1..4152a302411 100644
--- a/doc/api/vm.md
+++ b/doc/api/vm.md
@@ -1318,6 +1318,31 @@ added:
 
 A `ModuleRequest` represents the request to import a module with given import attributes and phase.
 
+## Class: `vm.MicrotaskQueue`
+
+<!-- YAML
+added: REPLACEME
+-->
+
+Represents an explicit microtask queue that can be shared across multiple
+`vm.Context` instances and synchronously drained by the embedder.
+
+### `new vm.MicrotaskQueue()`
+
+<!-- YAML
+added: REPLACEME
+-->
+
+Creates a new `vm.MicrotaskQueue` instance.
+
+### `microtaskQueue.runMicrotasks()`
+
+<!-- YAML
+added: REPLACEME
+-->
+
+Synchronously runs all microtasks currently queued in this microtask queue.
+
 ## `vm.compileFunction(code[, params[, options]])`
 
 <!-- YAML
@@ -1474,6 +1499,10 @@ changes:
     scheduled through `Promise`s and `async function`s) will be run immediately
     after a script has run through [`script.runInContext()`][].
     They are included in the `timeout` and `breakOnSigint` scopes in that case.
+  * `microtaskQueue` {vm.MicrotaskQueue} A microtask queue created with
+    [`new vm.MicrotaskQueue()`][] or [`vm.createMicrotaskQueue()`][]. If
+    specified, microtasks scheduled inside this context will be placed on this
+    queue, allowing multiple contexts to share the same microtask queue.
   * `importModuleDynamically`
     {Function|vm.constants.USE\_MAIN\_CONTEXT\_DEFAULT\_LOADER}
     Used to specify the how the modules should be loaded when `import()` is
@@ -1555,6 +1584,28 @@ Returns `true` if the given `object` object has been [contextified][] using
 [`vm.createContext()`][], or if it's the global object of a context created
 using [`vm.constants.DONT_CONTEXTIFY`][].
 
+## `vm.createMicrotaskQueue()`
+
+<!-- YAML
+added: REPLACEME
+-->
+
+* Returns: {vm.MicrotaskQueue}
+
+Creates a new [`vm.MicrotaskQueue`][] instance. Shortcut to
+`new vm.MicrotaskQueue()`.
+
+## `vm.isMicrotaskQueue(object)`
+
+<!-- YAML
+added: REPLACEME
+-->
+
+* `object` {any}
+* Returns: {boolean}
+
+Returns `true` if the given `object` is an instance of [`vm.MicrotaskQueue`][].
+
 ## `vm.measureMemory([options])`
 
 <!-- YAML
@@ -1823,6 +1874,10 @@ changes:
     scheduled through `Promise`s and `async function`s) will be run immediately
     after the script has run. They are included in the `timeout` and
     `breakOnSigint` scopes in that case.
+  * `microtaskQueue` {vm.MicrotaskQueue} A microtask queue created with
+    [`new vm.MicrotaskQueue()`][] or [`vm.createMicrotaskQueue()`][]. If
+    specified, microtasks scheduled inside the new context will be placed on
+    this queue.
 * Returns: {any} the result of the very last statement executed in the script.
 
 This method is a shortcut to
@@ -2594,3 +2649,6 @@ const { Script, SyntheticModule } = require('node:vm');
 [global object]: https://tc39.es/ecma262/#sec-global-object
 [indirect `eval()` call]: https://developer.mozilla.org/en-US/docs/Web/JavaScript/Reference/Global_Objects/eval#direct_and_indirect_eval
 [origin]: https://developer.mozilla.org/en-US/docs/Glossary/Origin
+[`new vm.MicrotaskQueue()`]: #new-vmmicrotaskqueue
+[`vm.MicrotaskQueue`]: #class-vmmicrotaskqueue
+[`vm.createMicrotaskQueue()`]: #vmcreatemicrotaskqueue
diff --git a/lib/vm.js b/lib/vm.js
index 2c7446af607..76802533218 100644
--- a/lib/vm.js
+++ b/lib/vm.js
@@ -32,6 +32,8 @@ const {
 
 const {
   ContextifyScript,
+  MicrotaskQueue: ContextifyMicrotaskQueue,
+  isMicrotaskQueue: _isMicrotaskQueue,
   makeContext,
   constants,
   measureMemory: _measureMemory,
@@ -82,6 +84,16 @@ function isContext(object) {
   return _isContext(object);
 }
 
+class MicrotaskQueue extends ContextifyMicrotaskQueue {}
+
+function createMicrotaskQueue() {
+  return new MicrotaskQueue();
+}
+
+function isMicrotaskQueue(object) {
+  return typeof object === 'object' && object !== null && _isMicrotaskQueue(object);
+}
+
 class Script extends ContextifyScript {
   constructor(code, options = kEmptyObject) {
     code = `${code}`;
@@ -202,6 +214,7 @@ function getContextOptions(options) {
     origin: options.contextOrigin,
     codeGeneration: undefined,
     microtaskMode: options.microtaskMode,
+    microtaskQueue: options.microtaskQueue ?? options.contextMicrotaskQueue,
   };
   if (contextOptions.name !== undefined)
     validateString(contextOptions.name, 'options.contextName');
@@ -235,6 +248,7 @@ function createContext(contextObject = { __proto__: ObjectPrototype }, options =
     origin,
     codeGeneration,
     microtaskMode,
+    microtaskQueue,
     importModuleDynamically,
   } = options;
 
@@ -255,12 +269,27 @@ function createContext(contextObject = { __proto__: ObjectPrototype }, options =
   validateOneOf(microtaskMode,
                 'options.microtaskMode',
                 ['afterEvaluate', undefined]);
-  const microtaskQueue = (microtaskMode === 'afterEvaluate');
+  if (microtaskQueue !== undefined && !isMicrotaskQueue(microtaskQueue)) {
+    throw new ERR_INVALID_ARG_TYPE(
+      'options.microtaskQueue',
+      'MicrotaskQueue',
+      microtaskQueue,
+    );
+  }
 
   const hostDefinedOptionId =
     getHostDefinedOptionId(importModuleDynamically, name);
 
-  const result = makeContext(contextObject, name, origin, strings, wasm, microtaskQueue, hostDefinedOptionId);
+  const result = makeContext(
+    contextObject,
+    name,
+    origin,
+    strings,
+    wasm,
+    microtaskQueue ?? (microtaskMode === 'afterEvaluate'),
+    hostDefinedOptionId,
+    microtaskMode === 'afterEvaluate',
+  );
   // Register the context scope callback after the context was initialized.
   registerImportModuleDynamically(result, importModuleDynamically);
   return result;
@@ -413,6 +442,9 @@ module.exports = {
   compileFunction,
   measureMemory,
   constants: vmConstants,
+  MicrotaskQueue,
+  createMicrotaskQueue,
+  isMicrotaskQueue,
 };
 
 // The vm module is patched to include vm.Module, vm.SourceTextModule
diff --git a/src/env_properties.h b/src/env_properties.h
index 886d4adba9f..42fd55201f5 100644
--- a/src/env_properties.h
+++ b/src/env_properties.h
@@ -460,6 +460,7 @@
   V(lock_info_template, v8::DictionaryTemplate)                                \
   V(lock_query_template, v8::DictionaryTemplate)                               \
   V(message_port_constructor_template, v8::FunctionTemplate)                   \
+  V(microtask_queue_constructor_template, v8::FunctionTemplate)                \
   V(module_wrap_constructor_template, v8::FunctionTemplate)                    \
   V(mx_record_template, v8::DictionaryTemplate)                                \
   V(naptr_record_template, v8::DictionaryTemplate)                             \
diff --git a/src/node_contextify.cc b/src/node_contextify.cc
index 8f9dddf53ca..82a5952951b 100644
--- a/src/node_contextify.cc
+++ b/src/node_contextify.cc
@@ -153,10 +153,10 @@ ContextifyContext* ContextifyContext::New(Environment* env,
 
   const SnapshotData* snapshot_data = env->isolate_data()->snapshot_data();
 
-  MicrotaskQueue* queue =
-      options->own_microtask_queue
-          ? options->own_microtask_queue.get()
-          : env->isolate()->GetCurrentContext()->GetMicrotaskQueue();
+  MicrotaskQueue* queue = options->own_microtask_queue.get();
+  if (queue == nullptr) queue = options->shared_microtask_queue.get();
+  if (queue == nullptr)
+    queue = env->isolate()->GetCurrentContext()->GetMicrotaskQueue();
 
   Local<Context> v8_context;
   if (!(CreateV8Context(env->isolate(), object_template, snapshot_data, queue)
@@ -178,7 +178,9 @@ ContextifyContext::ContextifyContext(Environment* env,
                                      ContextOptions* options)
     : microtask_queue_(options->own_microtask_queue
                            ? options->own_microtask_queue.release()
-                           : nullptr) {
+                           : nullptr),
+      shared_microtask_queue_(std::move(options->shared_microtask_queue)),
+      drain_after_evaluate_(options->drain_after_evaluate) {
   CppgcMixin::Wrap(this, env, wrapper);
 
   context_.Reset(env->isolate(), v8_context);
@@ -414,7 +416,7 @@ void ContextifyContext::MakeContext(const FunctionCallbackInfo<Value>& args) {
   Environment* env = Environment::GetCurrent(args);
   ContextOptions options;
 
-  CHECK_EQ(args.Length(), 7);
+  CHECK_GE(args.Length(), 7);
   Local<Object> sandbox;
   if (args[0]->IsObject()) {
     sandbox = args[0].As<Object>();
@@ -445,11 +447,20 @@ void ContextifyContext::MakeContext(const FunctionCallbackInfo<Value>& args) {
   if (args[5]->IsBoolean() && args[5]->BooleanValue(env->isolate())) {
     options.own_microtask_queue =
         MicrotaskQueue::New(env->isolate(), MicrotasksPolicy::kExplicit);
+    options.drain_after_evaluate = true;
+  } else if (args[5]->IsObject()) {
+    ContextifyMicrotaskQueue* queue;
+    ASSIGN_OR_RETURN_UNWRAP_CPPGC(&queue, args[5].As<Object>());
+    options.shared_microtask_queue = queue->microtask_queue();
   }
 
   CHECK(args[6]->IsSymbol());
   options.host_defined_options_id = args[6].As<Symbol>();
 
+  if (args.Length() > 7 && args[7]->IsBoolean()) {
+    options.drain_after_evaluate = args[7]->BooleanValue(env->isolate());
+  }
+
   TryCatchScope try_catch(env);
   ContextifyContext* context_ptr =
       ContextifyContext::New(env, sandbox, &options);
@@ -2027,6 +2038,81 @@ static void MeasureMemory(const FunctionCallbackInfo<Value>& args) {
   args.GetReturnValue().Set(promise);
 }
 
+void ContextifyMicrotaskQueue::CreatePerIsolateProperties(
+    IsolateData* isolate_data, Local<ObjectTemplate> target) {
+  Isolate* isolate = isolate_data->isolate();
+  Local<String> class_name = FIXED_ONE_BYTE_STRING(isolate, "MicrotaskQueue");
+
+  Local<FunctionTemplate> tmpl = NewFunctionTemplate(isolate, New);
+  tmpl->InstanceTemplate()->SetInternalFieldCount(
+      ContextifyMicrotaskQueue::kInternalFieldCount);
+  tmpl->SetClassName(class_name);
+  SetProtoMethod(isolate, tmpl, "runMicrotasks", RunMicrotasks);
+
+  target->Set(isolate, "MicrotaskQueue", tmpl);
+  SetMethod(isolate, target, "isMicrotaskQueue", IsMicrotaskQueue);
+  isolate_data->set_microtask_queue_constructor_template(tmpl);
+}
+
+void ContextifyMicrotaskQueue::RegisterExternalReferences(
+    ExternalReferenceRegistry* registry) {
+  registry->Register(New);
+  registry->Register(RunMicrotasks);
+  registry->Register(IsMicrotaskQueue);
+}
+
+ContextifyMicrotaskQueue* ContextifyMicrotaskQueue::New(
+    Environment* env, Local<Object> object) {
+  DCHECK_NOT_NULL(env->isolate()->GetCppHeap());
+  return cppgc::MakeGarbageCollected<ContextifyMicrotaskQueue>(
+      env->cppgc_allocation_handle(), env, object);
+}
+
+void ContextifyMicrotaskQueue::New(const FunctionCallbackInfo<Value>& args) {
+  Environment* env = Environment::GetCurrent(args);
+  CHECK(args.IsConstructCall());
+  New(env, args.This());
+}
+
+ContextifyMicrotaskQueue::ContextifyMicrotaskQueue(
+    Environment* env, Local<Object> object)
+    : microtask_queue_(
+          MicrotaskQueue::New(env->isolate(), MicrotasksPolicy::kExplicit)) {
+  CppgcMixin::Wrap(this, env, object);
+}
+
+bool ContextifyMicrotaskQueue::InstanceOf(Environment* env,
+                                          const Local<Value>& value) {
+  return !value.IsEmpty() &&
+         value->IsObject() &&
+         env->microtask_queue_constructor_template()->HasInstance(value);
+}
+
+void ContextifyMicrotaskQueue::RunMicrotasks(
+    const FunctionCallbackInfo<Value>& args) {
+  Environment* env = Environment::GetCurrent(args);
+  if (!ContextifyMicrotaskQueue::InstanceOf(env, args.This())) {
+    THROW_ERR_INVALID_THIS(
+        env,
+        "MicrotaskQueue methods can only be called on "
+        "MicrotaskQueue instances.");
+    return;
+  }
+  ContextifyMicrotaskQueue* queue;
+  ASSIGN_OR_RETURN_UNWRAP_CPPGC(&queue, args.This());
+  queue->microtask_queue_->PerformCheckpoint(args.GetIsolate());
+}
+
+void ContextifyMicrotaskQueue::IsMicrotaskQueue(
+    const FunctionCallbackInfo<Value>& args) {
+  Environment* env = Environment::GetCurrent(args);
+  bool is_queue =
+      args.Length() > 0 && args[0]->IsObject() && InstanceOf(env, args[0]) &&
+      CppgcMixin::Unwrap<ContextifyMicrotaskQueue>(args[0].As<Object>()) !=
+          nullptr;
+  args.GetReturnValue().Set(is_queue);
+}
+
 void CreatePerIsolateProperties(IsolateData* isolate_data,
                                 Local<ObjectTemplate> target) {
   Isolate* isolate = isolate_data->isolate();
@@ -2034,6 +2120,7 @@ void CreatePerIsolateProperties(IsolateData* isolate_data,
   ContextifyContext::CreatePerIsolateProperties(isolate_data, target);
   ContextifyScript::CreatePerIsolateProperties(isolate_data, target);
   ContextifyFunction::CreatePerIsolateProperties(isolate_data, target);
+  ContextifyMicrotaskQueue::CreatePerIsolateProperties(isolate_data, target);
 
   SetMethod(isolate, target, "runInterruptible", RunInterruptible);
 
@@ -2083,6 +2170,7 @@ void RegisterExternalReferences(ExternalReferenceRegistry* registry) {
   ContextifyContext::RegisterExternalReferences(registry);
   ContextifyScript::RegisterExternalReferences(registry);
   ContextifyFunction::RegisterExternalReferences(registry);
+  ContextifyMicrotaskQueue::RegisterExternalReferences(registry);
 
   registry->Register(CompileFunctionForCJSLoader);
   registry->Register(RunInterruptible);
diff --git a/src/node_contextify.h b/src/node_contextify.h
index 1066633daf6..63fcc0dfecf 100644
--- a/src/node_contextify.h
+++ b/src/node_contextify.h
@@ -19,6 +19,8 @@ struct ContextOptions {
   v8::Local<v8::Boolean> allow_code_gen_strings;
   v8::Local<v8::Boolean> allow_code_gen_wasm;
   std::unique_ptr<v8::MicrotaskQueue> own_microtask_queue;
+  std::shared_ptr<v8::MicrotaskQueue> shared_microtask_queue;
+  bool drain_after_evaluate = false;
   v8::Local<v8::Symbol> host_defined_options_id;
   bool vanilla = false;
 };
@@ -122,7 +124,9 @@ class ContextifyContext final : CPPGC_MIXIN(ContextifyContext) {
   }
 
   inline v8::MicrotaskQueue* microtask_queue() const {
-    return microtask_queue_.get();
+    if (!drain_after_evaluate_) return nullptr;
+    if (microtask_queue_) return microtask_queue_.get();
+    return shared_microtask_queue_.get();
   }
 
   template <typename T>
@@ -187,6 +191,36 @@ class ContextifyContext final : CPPGC_MIXIN(ContextifyContext) {
 
   v8::TracedReference<v8::Context> context_;
   std::unique_ptr<v8::MicrotaskQueue> microtask_queue_;
+  std::shared_ptr<v8::MicrotaskQueue> shared_microtask_queue_;
+  bool drain_after_evaluate_ = false;
+};
+
+class ContextifyMicrotaskQueue final : CPPGC_MIXIN(ContextifyMicrotaskQueue) {
+ public:
+  SET_CPPGC_NAME(ContextifyMicrotaskQueue)
+  DEFAULT_CPPGC_TRACE()
+  SET_NO_MEMORY_INFO()
+
+  ContextifyMicrotaskQueue(Environment* env, v8::Local<v8::Object> object);
+  ~ContextifyMicrotaskQueue() override = default;
+
+  static ContextifyMicrotaskQueue* New(Environment* env,
+                                       v8::Local<v8::Object> object);
+  static void New(const v8::FunctionCallbackInfo<v8::Value>& args);
+  static bool InstanceOf(Environment* env, const v8::Local<v8::Value>& value);
+  static void RunMicrotasks(const v8::FunctionCallbackInfo<v8::Value>& args);
+  static void IsMicrotaskQueue(const v8::FunctionCallbackInfo<v8::Value>& args);
+
+  static void CreatePerIsolateProperties(IsolateData* isolate_data,
+                                         v8::Local<v8::ObjectTemplate> target);
+  static void RegisterExternalReferences(ExternalReferenceRegistry* registry);
+
+  inline std::shared_ptr<v8::MicrotaskQueue> microtask_queue() const {
+    return microtask_queue_;
+  }
+
+ private:
+  std::shared_ptr<v8::MicrotaskQueue> microtask_queue_;
 };
 
 class ContextifyScript final : CPPGC_MIXIN(ContextifyScript) {
diff --git a/test/parallel/test-vm-shared-microtask-queue.js b/test/parallel/test-vm-shared-microtask-queue.js
new file mode 100644
index 00000000000..0ceb8452319
--- /dev/null
+++ b/test/parallel/test-vm-shared-microtask-queue.js
@@ -0,0 +1,141 @@
+'use strict';
+
+require('../common');
+const assert = require('assert');
+const vm = require('vm');
+
+// 1. Creation and type checking
+{
+  const queue1 = new vm.MicrotaskQueue();
+  const queue2 = vm.createMicrotaskQueue();
+
+  assert(vm.isMicrotaskQueue(queue1));
+  assert(vm.isMicrotaskQueue(queue2));
+  assert(queue1 instanceof vm.MicrotaskQueue);
+  assert(queue2 instanceof vm.MicrotaskQueue);
+
+  assert.strictEqual(vm.isMicrotaskQueue({}), false);
+  assert.strictEqual(vm.isMicrotaskQueue(null), false);
+  assert.strictEqual(vm.isMicrotaskQueue(undefined), false);
+  assert.strictEqual(vm.isMicrotaskQueue(42), false);
+  assert.strictEqual(vm.isMicrotaskQueue('queue'), false);
+
+  assert.throws(() => {
+    vm.MicrotaskQueue();
+  }, {
+    name: 'TypeError',
+    message: "Class constructor MicrotaskQueue cannot be invoked without 'new'",
+  });
+
+  assert.throws(() => {
+    queue1.runMicrotasks.call({});
+  }, {
+    code: 'ERR_INVALID_THIS',
+    name: 'TypeError',
+  });
+}
+
+// 2. Options validation
+{
+  assert.throws(() => {
+    vm.createContext({}, { microtaskQueue: {} });
+  }, {
+    code: 'ERR_INVALID_ARG_TYPE',
+    name: 'TypeError',
+  });
+
+  assert.throws(() => {
+    vm.runInNewContext('1 + 1', {}, { microtaskQueue: 'invalid' });
+  }, {
+    code: 'ERR_INVALID_ARG_TYPE',
+    name: 'TypeError',
+  });
+}
+
+// 3. The exact issue #65555 HTML Window and same-agent iframe checkpoint model
+{
+  function run(options, drain = () => {}) {
+    const trace = [];
+    const record = (entry) => trace.push(entry);
+    const window = vm.createContext({ record }, options);
+    const iframe = vm.createContext({ record }, options);
+
+    vm.runInContext(`
+      const pending = new Promise((resolve) => {
+        globalThis.resolve = resolve;
+      });
+      pending.then(() => {
+        record('win-rxn');
+        Promise.resolve().then(() => record('win-follow-up'));
+      });
+    `, window);
+
+    vm.runInContext(`
+      const pending = new Promise((resolve) => {
+        globalThis.resolve = resolve;
+      });
+      pending.then(() => record('iframe-rxn'));
+    `, iframe);
+
+    window.resolveIframe = iframe.resolve;
+    vm.runInContext('resolve(); resolveIframe();', window);
+    drain(iframe);
+
+    return trace;
+  }
+
+  const expected = ['win-rxn', 'iframe-rxn', 'win-follow-up'];
+
+  // Default contexts share Node's queue, but have not drained before returning
+  assert.deepStrictEqual(run(), []);
+
+  // afterEvaluate gives every context a separate queue, draining Window prematurely
+  assert.deepStrictEqual(
+    run(
+      { microtaskMode: 'afterEvaluate' },
+      (iframe) => vm.runInContext('', iframe),
+    ),
+    ['win-rxn', 'win-follow-up', 'iframe-rxn'],
+  );
+
+  // Shared microtask queue achieves the HTML specification order
+  const queue = vm.createMicrotaskQueue();
+  assert.deepStrictEqual(
+    run(
+      { microtaskQueue: queue },
+      () => queue.runMicrotasks(),
+    ),
+    expected,
+  );
+}
+
+// 4. Shared microtask queue with microtaskMode: 'afterEvaluate'
+{
+  const queue = new vm.MicrotaskQueue();
+  const trace = [];
+  const record = (entry) => trace.push(entry);
+
+  const contextA = vm.createContext({ record }, {
+    microtaskQueue: queue,
+    microtaskMode: 'afterEvaluate',
+  });
+  const contextB = vm.createContext({ record }, {
+    microtaskQueue: queue,
+  });
+
+  vm.runInContext(`
+    Promise.resolve().then(() => record('A'));
+  `, contextA);
+
+  vm.runInContext(`
+    Promise.resolve().then(() => record('B'));
+  `, contextB);
+
+  // Context A has afterEvaluate, so evaluation drains the shared queue
+  assert.deepStrictEqual(trace, ['A']);
+
+  // Context B does not have afterEvaluate, so microtasks stay until explicitly drained
+  assert.deepStrictEqual(trace, ['A']);
+  queue.runMicrotasks();
+  assert.deepStrictEqual(trace, ['A', 'B']);
+}