diff --git a/src/module_wrap.cc b/src/module_wrap.cc
index aa6b3bc303f..9b7354adfca 100644
--- a/src/module_wrap.cc
+++ b/src/module_wrap.cc
@@ -791,6 +791,8 @@ void ModuleWrap::Evaluate(const FunctionCallbackInfo<Value>& args) {
 
   bool timed_out = false;
   bool received_signal = false;
+  const uint32_t async_stack_length =
+      realm->env()->async_hooks()->fields()[AsyncHooks::kStackLength];
   MaybeLocal<Value> result;
   {
     auto wd = timeout != -1
@@ -853,6 +855,13 @@ void ModuleWrap::Evaluate(const FunctionCallbackInfo<Value>& args) {
   if (timed_out || received_signal) {
     if (!realm->env()->is_main_thread() && realm->env()->is_stopping()) return;
     isolate->CancelTerminateExecution();
+    // A promise job terminated by the watchdog never runs its async hook
+    // `after` callback, so drop the contexts it left on the stack.
+    AsyncHooks* async_hooks = realm->env()->async_hooks();
+    while (async_hooks->fields()[AsyncHooks::kStackLength] >
+           async_stack_length) {
+      async_hooks->pop_async_context(realm->env()->execution_async_id());
+    }
     // It is possible that execution was terminated by another timeout in
     // which this timeout is nested, so check whether one of the watchdogs
     // from this invocation is responsible for termination.
diff --git a/src/node_contextify.cc b/src/node_contextify.cc
index 838a65c1ff3..11939e4002b 100644
--- a/src/node_contextify.cc
+++ b/src/node_contextify.cc
@@ -1286,6 +1286,8 @@ bool ContextifyScript::EvalMachine(Local<Context> context,
   MaybeLocal<Value> result;
   bool timed_out = false;
   bool received_signal = false;
+  const uint32_t async_stack_length =
+      env->async_hooks()->fields()[AsyncHooks::kStackLength];
   {
     auto wd = timeout != -1 ? std::make_optional<Watchdog>(
                                   env->isolate(), timeout, &timed_out)
@@ -1304,6 +1306,13 @@ bool ContextifyScript::EvalMachine(Local<Context> context,
     if (!env->is_main_thread() && env->is_stopping())
       return false;
     env->isolate()->CancelTerminateExecution();
+    // A promise job terminated by the watchdog never runs its async hook
+    // `after` callback, so drop the contexts it left on the stack.
+    AsyncHooks* async_hooks = env->async_hooks();
+    while (async_hooks->fields()[AsyncHooks::kStackLength] >
+           async_stack_length) {
+      async_hooks->pop_async_context(env->execution_async_id());
+    }
     // It is possible that execution was terminated by another timeout in
     // which this timeout is nested, so check whether one of the watchdogs
     // from this invocation is responsible for termination.
diff --git a/test/parallel/test-async-hooks-vm-module-timeout.js b/test/parallel/test-async-hooks-vm-module-timeout.js
new file mode 100644
index 00000000000..ecfe2f2e31a
--- /dev/null
+++ b/test/parallel/test-async-hooks-vm-module-timeout.js
@@ -0,0 +1,23 @@
+// Flags: --experimental-vm-modules
+'use strict';
+
+const common = require('../common');
+const assert = require('assert');
+const async_hooks = require('async_hooks');
+const vm = require('vm');
+
+async_hooks.createHook({ init() {} }).enable();
+
+(async () => {
+  const context = vm.createContext({}, { microtaskMode: 'afterEvaluate' });
+  const module = new vm.SourceTextModule(
+    'Promise.resolve().then(() => { while (true); });',
+    { context }
+  );
+  await module.link(common.mustNotCall());
+
+  await assert.rejects(module.evaluate({ timeout: 5 }), {
+    code: 'ERR_SCRIPT_EXECUTION_TIMEOUT',
+  });
+  setImmediate(common.mustCall());
+})().then(common.mustCall());
diff --git a/test/parallel/test-async-hooks-vm-timeout.js b/test/parallel/test-async-hooks-vm-timeout.js
new file mode 100644
index 00000000000..4b2261ea1b0
--- /dev/null
+++ b/test/parallel/test-async-hooks-vm-timeout.js
@@ -0,0 +1,24 @@
+'use strict';
+
+const common = require('../common');
+const assert = require('assert');
+const async_hooks = require('async_hooks');
+const vm = require('vm');
+
+async_hooks.createHook({ init() {} }).enable();
+
+const executionAsyncId = async_hooks.executionAsyncId();
+const context = vm.createContext({}, { microtaskMode: 'afterEvaluate' });
+
+assert.throws(() => {
+  vm.runInContext(
+    'Promise.resolve().then(() => { while (true); });',
+    context,
+    { timeout: 5 }
+  );
+}, {
+  code: 'ERR_SCRIPT_EXECUTION_TIMEOUT',
+});
+
+assert.strictEqual(async_hooks.executionAsyncId(), executionAsyncId);
+setImmediate(common.mustCall());