diff --git a/scene/gui/popup_menu.cpp b/scene/gui/popup_menu.cpp
index 79ff3b07c24..864896b6442 100644
--- a/scene/gui/popup_menu.cpp
+++ b/scene/gui/popup_menu.cpp
@@ -478,11 +478,15 @@ void PopupMenu::_input_from_window_internal(const Ref<InputEvent> &p_event) {
 		Ref<InputEventJoypadButton> joypadbutton_event = p_event;
 		bool is_joypad_event = (joypadmotion_event.is_valid() || joypadbutton_event.is_valid());
 
+		if (is_joypad_event && !has_focus_or_active_popup()) {
+			return;
+		}
 		if (p_event->is_action("ui_down", true) && p_event->is_pressed()) {
 			if (is_joypad_event) {
 				if (!input->is_action_just_pressed("ui_down", true)) {
 					return;
 				}
+				joypad_event_process = true;
 				set_process_internal(true);
 			}
 			int search_from = mouse_over + 1;
@@ -525,6 +529,7 @@ void PopupMenu::_input_from_window_internal(const Ref<InputEvent> &p_event) {
 				if (!input->is_action_just_pressed("ui_up", true)) {
 					return;
 				}
+				joypad_event_process = true;
 				set_process_internal(true);
 			}
 			int search_from = mouse_over - 1;
@@ -1291,76 +1296,79 @@ void PopupMenu::_notification(int p_what) {
 		case NOTIFICATION_INTERNAL_PROCESS: {
 			Input *input = Input::get_singleton();
 
-			if (input->is_action_just_released("ui_up") || input->is_action_just_released("ui_down")) {
-				gamepad_event_delay_ms = DEFAULT_GAMEPAD_EVENT_DELAY_MS;
-				set_process_internal(false);
-				return;
-			}
-			gamepad_event_delay_ms -= get_process_delta_time();
-			if (gamepad_event_delay_ms <= 0) {
-				if (input->is_action_pressed("ui_down")) {
-					gamepad_event_delay_ms = GAMEPAD_EVENT_REPEAT_RATE_MS + gamepad_event_delay_ms;
-					int search_from = mouse_over + 1;
-					if (search_from >= items.size()) {
-						search_from = 0;
-					}
+			if (joypad_event_process && has_focus_or_active_popup()) {
+				if (input->is_action_just_released("ui_up") || input->is_action_just_released("ui_down")) {
+					gamepad_event_delay_ms = DEFAULT_GAMEPAD_EVENT_DELAY_MS;
+					set_process_internal(false);
+					return;
+				}
 
-					bool match_found = false;
-					for (int i = search_from; i < items.size(); i++) {
-						if (!items[i].separator && !items[i].disabled) {
-							mouse_over = i;
-							emit_signal(SNAME("id_focused"), items[i].id);
-							scroll_to_item(i);
-							control->queue_redraw();
-							match_found = true;
-							break;
+				gamepad_event_delay_ms -= get_process_delta_time();
+				if (gamepad_event_delay_ms <= 0) {
+					if (input->is_action_pressed("ui_down")) {
+						gamepad_event_delay_ms = GAMEPAD_EVENT_REPEAT_RATE_MS + gamepad_event_delay_ms;
+						int search_from = mouse_over + 1;
+						if (search_from >= items.size()) {
+							search_from = 0;
 						}
-					}
 
-					if (!match_found) {
-						// If the last item is not selectable, try re-searching from the start.
-						for (int i = 0; i < search_from; i++) {
+						bool match_found = false;
+						for (int i = search_from; i < items.size(); i++) {
 							if (!items[i].separator && !items[i].disabled) {
 								mouse_over = i;
 								emit_signal(SNAME("id_focused"), items[i].id);
 								scroll_to_item(i);
 								control->queue_redraw();
+								match_found = true;
 								break;
 							}
 						}
-					}
-				}
 
-				if (input->is_action_pressed("ui_up")) {
-					gamepad_event_delay_ms = GAMEPAD_EVENT_REPEAT_RATE_MS + gamepad_event_delay_ms;
-					int search_from = mouse_over - 1;
-					if (search_from < 0) {
-						search_from = items.size() - 1;
-					}
-
-					bool match_found = false;
-					for (int i = search_from; i >= 0; i--) {
-						if (!items[i].separator && !items[i].disabled) {
-							mouse_over = i;
-							emit_signal(SNAME("id_focused"), items[i].id);
-							scroll_to_item(i);
-							control->queue_redraw();
-							match_found = true;
-							break;
+						if (!match_found) {
+							// If the last item is not selectable, try re-searching from the start.
+							for (int i = 0; i < search_from; i++) {
+								if (!items[i].separator && !items[i].disabled) {
+									mouse_over = i;
+									emit_signal(SNAME("id_focused"), items[i].id);
+									scroll_to_item(i);
+									control->queue_redraw();
+									break;
+								}
+							}
 						}
 					}
 
-					if (!match_found) {
-						// If the first item is not selectable, try re-searching from the end.
-						for (int i = items.size() - 1; i >= search_from; i--) {
+					if (input->is_action_pressed("ui_up")) {
+						gamepad_event_delay_ms = GAMEPAD_EVENT_REPEAT_RATE_MS + gamepad_event_delay_ms;
+						int search_from = mouse_over - 1;
+						if (search_from < 0) {
+							search_from = items.size() - 1;
+						}
+
+						bool match_found = false;
+						for (int i = search_from; i >= 0; i--) {
 							if (!items[i].separator && !items[i].disabled) {
 								mouse_over = i;
 								emit_signal(SNAME("id_focused"), items[i].id);
 								scroll_to_item(i);
 								control->queue_redraw();
+								match_found = true;
 								break;
 							}
 						}
+
+						if (!match_found) {
+							// If the first item is not selectable, try re-searching from the end.
+							for (int i = items.size() - 1; i >= search_from; i--) {
+								if (!items[i].separator && !items[i].disabled) {
+									mouse_over = i;
+									emit_signal(SNAME("id_focused"), items[i].id);
+									scroll_to_item(i);
+									control->queue_redraw();
+									break;
+								}
+							}
+						}
 					}
 				}
 			}
@@ -1408,6 +1416,7 @@ void PopupMenu::_notification(int p_what) {
 				}
 			} else {
 				if (!is_embedded()) {
+					joypad_event_process = false;
 					set_process_internal(true);
 				}
 
diff --git a/scene/gui/popup_menu.h b/scene/gui/popup_menu.h
index f4f534b097e..bd7c2214082 100644
--- a/scene/gui/popup_menu.h
+++ b/scene/gui/popup_menu.h
@@ -168,6 +168,7 @@ class PopupMenu : public Popup {
 	const float DEFAULT_GAMEPAD_EVENT_DELAY_MS = 0.5;
 	const float GAMEPAD_EVENT_REPEAT_RATE_MS = 1.0 / 20;
 	float gamepad_event_delay_ms = DEFAULT_GAMEPAD_EVENT_DELAY_MS;
+	bool joypad_event_process = false;
 
 	struct ThemeCache {
 		Ref<StyleBox> panel_style;
diff --git a/scene/main/window.cpp b/scene/main/window.cpp
index ec04feca747..4b0e4dbc0a5 100644
--- a/scene/main/window.cpp
+++ b/scene/main/window.cpp
@@ -2111,6 +2111,14 @@ bool Window::has_focus() const {
 	return focused;
 }
 
+bool Window::has_focus_or_active_popup() const {
+	ERR_READ_THREAD_GUARD_V(false);
+	if (window_id != DisplayServer::INVALID_WINDOW_ID) {
+		return DisplayServer::get_singleton()->window_is_focused(window_id) || (DisplayServer::get_singleton()->window_get_active_popup() == window_id);
+	}
+	return focused;
+}
+
 void Window::start_drag() {
 	ERR_MAIN_THREAD_GUARD;
 	if (window_id != DisplayServer::INVALID_WINDOW_ID) {
diff --git a/scene/main/window.h b/scene/main/window.h
index bebd77eeceb..444019cb440 100644
--- a/scene/main/window.h
+++ b/scene/main/window.h
@@ -419,6 +419,7 @@ public:
 
 	void grab_focus();
 	bool has_focus() const;
+	bool has_focus_or_active_popup() const;
 
 	void start_drag();
 	void start_resize(DisplayServer::WindowResizeEdge p_edge);