diff --git a/src/gui_gtk4.c b/src/gui_gtk4.c
index 083ac9f4001f9..14c7f7c538d89 100644
--- a/src/gui_gtk4.c
+++ b/src/gui_gtk4.c
@@ -282,6 +282,9 @@ static void leave_notify_event(GtkEventControllerMotion *controller, gpointer da
 static gboolean scroll_event(GtkEventControllerScroll *controller, double dx, double dy, gpointer data);
 static void focus_in_event(GtkEventControllerFocus *controller, gpointer data);
 static void focus_out_event(GtkEventControllerFocus *controller, gpointer data);
+#ifdef FEAT_MENU
+static gboolean menubar_popover_closed_hook(GSignalInvocationHint *ihint, guint n_param_values, const GValue *param_values, gpointer data);
+#endif
 #ifdef FEAT_DND
 static gboolean drop_cb(GtkDropTarget *target, const GValue *value, double x, double y, gpointer data);
 #endif
@@ -472,6 +475,20 @@ gui_mch_init(void)
 	gtk_widget_set_visible(gui.menubar, FALSE);
 	gtk_box_append(GTK_BOX(vbox), gui.menubar);
     }
+    // Return keyboard focus to the drawing area when a menubar popover
+    // closes (issue #20274).  GtkPopoverMenuBar owns its popovers
+    // privately, so attach via an emission hook on GtkPopover::closed
+    // and filter for popovers under our menubar inside the callback.
+    {
+	GTypeClass *cls = g_type_class_ref(GTK_TYPE_POPOVER);
+	guint sig_id = g_signal_lookup("closed", GTK_TYPE_POPOVER);
+
+	if (sig_id != 0)
+	    g_signal_add_emission_hook(sig_id, 0,
+		    menubar_popover_closed_hook, NULL, NULL);
+	if (cls != NULL)
+	    g_type_class_unref(cls);
+    }
 #endif
 
 #ifdef FEAT_TOOLBAR
@@ -1841,6 +1858,48 @@ focus_out_event(GtkEventControllerFocus *controller UNUSED,
 	gui_mch_stop_blink(TRUE);
 }
 
+#ifdef FEAT_MENU
+    static gboolean
+grab_drawarea_focus_idle(gpointer data UNUSED)
+{
+    if (gui.drawarea != NULL && !gtk_widget_has_focus(gui.drawarea))
+	gtk_widget_grab_focus(gui.drawarea);
+    return G_SOURCE_REMOVE;
+}
+
+    static gboolean
+menubar_popover_closed_hook(GSignalInvocationHint *ihint UNUSED,
+	guint n_param_values, const GValue *param_values,
+	gpointer data UNUSED)
+{
+    GObject	*obj;
+    GtkWidget	*popover;
+    GtkWidget	*parent;
+
+    if (n_param_values < 1 || gui.menubar == NULL || gui.drawarea == NULL)
+	return TRUE;
+    obj = g_value_get_object(&param_values[0]);
+    if (!GTK_IS_POPOVER(obj))
+	return TRUE;
+    popover = GTK_WIDGET(obj);
+
+    // Only react to popovers that descend from the menubar.
+    for (parent = gtk_widget_get_parent(popover);
+	    parent != NULL;
+	    parent = gtk_widget_get_parent(parent))
+    {
+	if (parent != gui.menubar)
+	    continue;
+	// Defer the grab to the next main loop iteration; calling it
+	// synchronously while GTK is still completing the popover close
+	// has no effect (issue #20274).
+	g_idle_add(grab_drawarea_focus_idle, NULL);
+	break;
+    }
+    return TRUE;	// keep the emission hook installed
+}
+#endif
+
     static void
 drawarea_realize_cb(GtkWidget *widget UNUSED, gpointer data UNUSED)
 {