diff --git a/atom/browser/api/atom_api_menu_views.cc b/atom/browser/api/atom_api_menu_views.cc
index 0a3b161830..2511f9765e 100644
--- a/atom/browser/api/atom_api_menu_views.cc
+++ b/atom/browser/api/atom_api_menu_views.cc
@@ -48,7 +48,7 @@ void MenuViews::PopupAt(Window* window, int x, int y, int positioning_item) {
   // Show the menu.
   int32_t window_id = window->ID();
   auto close_callback = base::Bind(
-      &MenuViews::ClosePopupAt, weak_factory_.GetWeakPtr(), window_id);
+      &MenuViews::OnClosed, weak_factory_.GetWeakPtr(), window_id);
   menu_runners_[window_id] = std::unique_ptr<MenuRunner>(new MenuRunner(
       model(), flags, close_callback));
   menu_runners_[window_id]->RunMenuAt(
@@ -60,12 +60,23 @@ void MenuViews::PopupAt(Window* window, int x, int y, int positioning_item) {
 }
 
 void MenuViews::ClosePopupAt(int32_t window_id) {
-  if (menu_runners_[window_id]) {
-    menu_runners_[window_id]->Cancel();
-    menu_runners_.erase(window_id);
+  auto runner = menu_runners_.find(window_id);
+  if (runner != menu_runners_.end()) {
+    // Close the runner for the window.
+    runner->second->Cancel();
+  } else if (window_id == -1) {
+    // Or just close all opened runners.
+    for (auto it = menu_runners_.begin(); it != menu_runners_.end();) {
+      // The iterator is invalidated after the call.
+      (it++)->second->Cancel();
+    }
   }
 }
 
+void MenuViews::OnClosed(int32_t window_id) {
+  menu_runners_.erase(window_id);
+}
+
 // static
 mate::WrappableBase* Menu::New(mate::Arguments* args) {
   return new MenuViews(args->isolate(), args->GetThis());
diff --git a/atom/browser/api/atom_api_menu_views.h b/atom/browser/api/atom_api_menu_views.h
index d0c33b3960..190e7d1cdf 100644
--- a/atom/browser/api/atom_api_menu_views.h
+++ b/atom/browser/api/atom_api_menu_views.h
@@ -25,6 +25,8 @@ class MenuViews : public Menu {
   void ClosePopupAt(int32_t window_id) override;
 
  private:
+  void OnClosed(int32_t window_id);
+
   // window ID -> open context menu
   std::map<int32_t, std::unique_ptr<views::MenuRunner>> menu_runners_;
 
diff --git a/lib/browser/api/menu.js b/lib/browser/api/menu.js
index bd3427bcd6..4713d62194 100644
--- a/lib/browser/api/menu.js
+++ b/lib/browser/api/menu.js
@@ -94,10 +94,13 @@ Menu.prototype.popup = function (window, x, y, positioningItem) {
 }
 
 Menu.prototype.closePopup = function (window) {
-  if (!window || window.constructor !== BrowserWindow) {
-    window = BrowserWindow.getFocusedWindow()
+  if (window && window.constructor !== BrowserWindow) {
+    this.closePopupAt(window.id)
+  } else {
+    // Passing -1 (invalid) would make closePopupAt close the all menu runners
+    // belong to this menu.
+    this.closePopupAt(-1)
   }
-  if (window) this.closePopupAt(window.id)
 }
 
 Menu.prototype.getMenuItemById = function (id) {