diff --git a/Userland/Libraries/LibJS/Interpreter.cpp b/Userland/Libraries/LibJS/Interpreter.cpp
index 9bbb929e91..f3bd3685e9 100644
--- a/Userland/Libraries/LibJS/Interpreter.cpp
+++ b/Userland/Libraries/LibJS/Interpreter.cpp
@@ -54,11 +54,17 @@ void Interpreter::run(GlobalObject& global_object, const Program& program)
     vm.push_call_frame(global_call_frame, global_object);
     VERIFY(!vm.exception());
     program.execute(*this, global_object);
+
+    // Whatever the promise jobs or on_call_stack_emptied do should not affect the effective
+    // 'last value'.
+    auto last_value = vm.last_value();
+
     vm.pop_call_frame();
 
-    // Whatever the promise jobs do should not affect the effective 'last value'.
-    auto last_value = vm.last_value();
+    // At this point we may have already run any queued promise jobs via on_call_stack_emptied,
+    // in which case this is a no-op.
     vm.run_queued_promise_jobs();
+
     vm.set_last_value({}, last_value.value_or(js_undefined()));
 }
 
diff --git a/Userland/Libraries/LibJS/Runtime/VM.h b/Userland/Libraries/LibJS/Runtime/VM.h
index d154414b46..e9e8c8f823 100644
--- a/Userland/Libraries/LibJS/Runtime/VM.h
+++ b/Userland/Libraries/LibJS/Runtime/VM.h
@@ -106,7 +106,12 @@ public:
             m_call_stack.append(&call_frame);
     }
 
-    void pop_call_frame() { m_call_stack.take_last(); }
+    void pop_call_frame()
+    {
+        m_call_stack.take_last();
+        if (m_call_stack.is_empty() && on_call_stack_emptied)
+            on_call_stack_emptied();
+    }
 
     CallFrame& call_frame() { return *m_call_stack.last(); }
     const CallFrame& call_frame() const { return *m_call_stack.last(); }
@@ -229,6 +234,7 @@ public:
 
     void promise_rejection_tracker(const Promise&, Promise::RejectionOperation) const;
 
+    AK::Function<void()> on_call_stack_emptied;
     AK::Function<void(const Promise&)> on_promise_unhandled_rejection;
     AK::Function<void(const Promise&)> on_promise_rejection_handled;
 
diff --git a/Userland/Libraries/LibWeb/DOM/Document.cpp b/Userland/Libraries/LibWeb/DOM/Document.cpp
index 3e3e8e82a2..e0cffb8965 100644
--- a/Userland/Libraries/LibWeb/DOM/Document.cpp
+++ b/Userland/Libraries/LibWeb/DOM/Document.cpp
@@ -560,6 +560,10 @@ JS::Interpreter& Document::interpreter()
         auto& vm = Bindings::main_thread_vm();
         // TODO: Hook up vm.on_promise_unhandled_rejection and vm.on_promise_rejection_handled
         // See https://developer.mozilla.org/en-US/docs/Web/JavaScript/Guide/Using_promises#promise_rejection_events
+        vm.on_call_stack_emptied = [this] {
+            auto& vm = m_interpreter->vm();
+            vm.run_queued_promise_jobs();
+        };
         m_interpreter = JS::Interpreter::create<Bindings::WindowObject>(vm, *m_window);
     }
     return *m_interpreter;
diff --git a/Userland/Libraries/LibWeb/DOM/EventDispatcher.cpp b/Userland/Libraries/LibWeb/DOM/EventDispatcher.cpp
index 7d4e73616c..78eccef06a 100644
--- a/Userland/Libraries/LibWeb/DOM/EventDispatcher.cpp
+++ b/Userland/Libraries/LibWeb/DOM/EventDispatcher.cpp
@@ -94,8 +94,6 @@ bool EventDispatcher::inner_invoke(Event& event, Vector<EventTarget::EventListen
             vm.clear_exception();
             // FIXME: Set legacyOutputDidListenersThrowFlag if given. (Only used by IndexedDB currently)
         }
-        vm.run_queued_promise_jobs();
-        VERIFY(!vm.exception());
 
         event.set_in_passive_listener(false);
         if (is<Bindings::WindowObject>(global)) {
diff --git a/Userland/Libraries/LibWeb/DOM/Window.cpp b/Userland/Libraries/LibWeb/DOM/Window.cpp
index 1b9f70e320..a5fc6fe89b 100644
--- a/Userland/Libraries/LibWeb/DOM/Window.cpp
+++ b/Userland/Libraries/LibWeb/DOM/Window.cpp
@@ -90,8 +90,6 @@ void Window::timer_did_fire(Badge<Timer>, Timer& timer)
     [[maybe_unused]] auto rc = vm.call(timer.callback(), wrapper());
     if (vm.exception())
         vm.clear_exception();
-    vm.run_queued_promise_jobs();
-    VERIFY(!vm.exception());
 }
 
 i32 Window::allocate_timer_id(Badge<Timer>)
@@ -126,8 +124,6 @@ i32 Window::request_animation_frame(JS::Function& callback)
         [[maybe_unused]] auto rc = vm.call(function, JS::js_undefined(), JS::Value(fake_timestamp));
         if (vm.exception())
             vm.clear_exception();
-        vm.run_queued_promise_jobs();
-        VERIFY(!vm.exception());
         GUI::DisplayLink::unregister_callback(link_id);
     });