diff --git a/editor/gui/editor_title_bar.cpp b/editor/gui/editor_title_bar.cpp
index c251c70c6de9..ba406e6704b1 100644
--- a/editor/gui/editor_title_bar.cpp
+++ b/editor/gui/editor_title_bar.cpp
@@ -40,7 +40,7 @@ void EditorTitleBar::gui_input(const Ref<InputEvent> &p_event) {
 		if (mm->get_button_mask().has_flag(MouseButtonMask::LEFT)) {
 			Window *w = Object::cast_to<Window>(get_viewport());
 			if (w) {
-				Point2 mouse = DisplayServer::get_singleton()->mouse_get_position();
+				Point2 mouse = get_viewport()->get_embedder_mouse_position();
 				w->set_position(mouse - click_pos);
 			}
 		} else {
@@ -54,7 +54,7 @@ void EditorTitleBar::gui_input(const Ref<InputEvent> &p_event) {
 		if (w) {
 			if (mb->get_button_index() == MouseButton::LEFT) {
 				if (mb->is_pressed()) {
-					click_pos = DisplayServer::get_singleton()->mouse_get_position() - w->get_position();
+					click_pos = get_viewport()->get_embedder_mouse_position() - w->get_position();
 					moving = true;
 				} else {
 					moving = false;
diff --git a/scene/gui/color_picker.cpp b/scene/gui/color_picker.cpp
index 9d245959169c..7012799a47ee 100644
--- a/scene/gui/color_picker.cpp
+++ b/scene/gui/color_picker.cpp
@@ -122,6 +122,7 @@ void ColorPicker::_notification(int p_what) {
 			if (!is_picking_color) {
 				return;
 			}
+			// This is only executed if previously is was checked, that the DisplayServer supports these functions.
 			set_pick_color(DisplayServer::get_singleton()->screen_get_pixel(DisplayServer::get_singleton()->mouse_get_position()));
 		}
 	}
diff --git a/scene/gui/popup_menu.cpp b/scene/gui/popup_menu.cpp
index dc586e86c931..436352fb41de 100644
--- a/scene/gui/popup_menu.cpp
+++ b/scene/gui/popup_menu.cpp
@@ -398,20 +398,8 @@ void PopupMenu::_activate_submenu(int p_over, bool p_by_keyboard) {
 
 void PopupMenu::_parent_focused() {
 	if (is_embedded()) {
-		Point2 mouse_pos_adjusted;
-		Window *window_parent = Object::cast_to<Window>(get_parent()->get_viewport());
-		while (window_parent) {
-			if (!window_parent->is_embedded()) {
-				mouse_pos_adjusted += window_parent->get_position();
-				break;
-			}
-
-			window_parent = Object::cast_to<Window>(window_parent->get_parent()->get_viewport());
-		}
-
 		Rect2 safe_area = get_embedder()->subwindow_get_popup_safe_rect(this);
-		Point2 pos = DisplayServer::get_singleton()->mouse_get_position() - mouse_pos_adjusted;
-		if (safe_area == Rect2i() || !safe_area.has_point(pos)) {
+		if (safe_area == Rect2i() || !safe_area.has_point(get_embedder_mouse_position())) {
 			Popup::_parent_focused();
 		} else {
 			grab_focus();
@@ -1127,7 +1115,7 @@ void PopupMenu::_notification(int p_what) {
 
 			// Only used when using operating system windows.
 			if (!activated_by_keyboard && !is_embedded() && autohide_areas.size()) {
-				Point2 mouse_pos = DisplayServer::get_singleton()->mouse_get_position();
+				Point2 mouse_pos = get_embedder_mouse_position();
 				mouse_pos -= get_position();
 
 				for (const Rect2 &E : autohide_areas) {
diff --git a/scene/main/viewport.cpp b/scene/main/viewport.cpp
index 5999b85988e3..ce8706683133 100644
--- a/scene/main/viewport.cpp
+++ b/scene/main/viewport.cpp
@@ -1398,10 +1398,41 @@ Vector2 Viewport::get_mouse_position() const {
 		return xform.affine_inverse().xform(DisplayServer::get_singleton()->mouse_get_position());
 	} else {
 		// Fallback to Input for getting mouse position in case of emulated mouse.
+		// Reports wrong coordinates, when used in an unfocused native Window.
 		return get_screen_transform_internal().affine_inverse().xform(Input::get_singleton()->get_mouse_position());
 	}
 }
 
+Vector2 Viewport::get_embedder_mouse_position() const {
+	// Return the mouse position in the coordinate system of the Viewport, where this is embedded.
+	// If this is a non-embedded Window, return the mouse position of the DisplayServer, if it supports it.
+	ERR_READ_THREAD_GUARD_V(Vector2());
+
+	const Window *w = Object::cast_to<Window>(this);
+	if (w) {
+		Viewport *e = w->get_embedder();
+		if (e) {
+			return e->get_mouse_position();
+		}
+		// Viewport is a native Window.
+		if (DisplayServer::get_singleton()->has_feature(DisplayServer::FEATURE_MOUSE)) {
+			return DisplayServer::get_singleton()->mouse_get_position();
+		}
+		// Fallback to Input for getting mouse position in case of emulated mouse.
+		// Reports wrong coordinates, when used in an unfocused native Window.
+		return Input::get_singleton()->get_mouse_position();
+	}
+
+	// This is a SubViewport.
+	Window *b = get_base_window();
+	if (b) {
+		return b->get_embedder_mouse_position();
+	}
+
+	// Case that SubViewport is not directly attached to screen.
+	return gui.last_mouse_pos;
+}
+
 void Viewport::warp_mouse(const Vector2 &p_position) {
 	ERR_MAIN_THREAD_GUARD;
 	Transform2D xform = get_screen_transform_internal();
@@ -2556,6 +2587,10 @@ Window *Viewport::get_base_window() const {
 	Viewport *v = const_cast<Viewport *>(this);
 	Window *w = Object::cast_to<Window>(v);
 	while (!w) {
+		if (!Object::cast_to<SubViewportContainer>(v->get_parent())) {
+			// In this case there is no meaningful Window to return.
+			return nullptr;
+		}
 		v = v->get_parent_viewport();
 		w = Object::cast_to<Window>(v);
 	}
diff --git a/scene/main/viewport.h b/scene/main/viewport.h
index 43a89c8a0b1b..4eb2fb8ea907 100644
--- a/scene/main/viewport.h
+++ b/scene/main/viewport.h
@@ -595,6 +595,7 @@ class Viewport : public Node {
 	bool is_input_disabled() const;
 
 	Vector2 get_mouse_position() const;
+	Vector2 get_embedder_mouse_position() const;
 	void warp_mouse(const Vector2 &p_position);
 	virtual void update_mouse_cursor_state();