diff --git a/src/core/display-private.h b/src/core/display-private.h
index daa12a573..4afd0d5df 100644
--- a/src/core/display-private.h
+++ b/src/core/display-private.h
@@ -297,6 +297,9 @@ void meta_display_cancel_touch (MetaDisplay *display);
 
 gboolean meta_display_windows_are_interactable (MetaDisplay *display);
 
+void meta_display_queue_focus (MetaDisplay *display,
+                               MetaWindow  *window);
+
 void meta_display_show_tablet_mapping_notification (MetaDisplay        *display,
                                                     ClutterInputDevice *pad,
                                                     const gchar        *pretty_name);
diff --git a/src/core/display.c b/src/core/display.c
index 652bd97ef..e9ff7ba55 100644
--- a/src/core/display.c
+++ b/src/core/display.c
@@ -141,6 +141,11 @@ typedef struct _MetaDisplayPrivate
   GList *queue_windows[META_N_QUEUE_TYPES];
 
   gboolean enable_input_capture;
+
+  struct {
+    MetaWindow *window;
+    gulong unmanaging_handler_id;
+  } focus_on_grab_dismissed;
 } MetaDisplayPrivate;
 
 G_DEFINE_TYPE_WITH_PRIVATE (MetaDisplay, meta_display, G_TYPE_OBJECT)
@@ -209,6 +214,10 @@ meta_display_show_osd (MetaDisplay *display,
                        const gchar *icon_name,
                        const gchar *message);
 
+static void on_is_grabbed_changed (ClutterStage *stage,
+                                   GParamSpec   *pspec,
+                                   MetaDisplay  *display);
+
 static MetaBackend *
 backend_from_display (MetaDisplay *display)
 {
@@ -917,6 +926,7 @@ meta_display_new (MetaContext  *context,
                   GError      **error)
 {
   MetaBackend *backend = meta_context_get_backend (context);
+  ClutterActor *stage = meta_backend_get_stage (backend);
   MetaDisplay *display;
   MetaDisplayPrivate *priv;
   guint32 timestamp;
@@ -1091,6 +1101,8 @@ meta_display_new (MetaContext  *context,
   meta_display_unset_input_focus (display, timestamp);
 #endif
 
+  g_signal_connect (stage, "notify::is-grabbed",
+                    G_CALLBACK (on_is_grabbed_changed), display);
 
   display->sound_player = g_object_new (META_TYPE_SOUND_PLAYER, NULL);
 
@@ -1315,6 +1327,52 @@ meta_display_windows_are_interactable (MetaDisplay *display)
   return TRUE;
 }
 
+static void
+on_is_grabbed_changed (ClutterStage *stage,
+                       GParamSpec   *pspec,
+                       MetaDisplay  *display)
+{
+  MetaDisplayPrivate *priv = meta_display_get_instance_private (display);
+
+  if (!priv->focus_on_grab_dismissed.window)
+    return;
+
+  meta_window_focus (priv->focus_on_grab_dismissed.window, META_CURRENT_TIME);
+
+  g_clear_signal_handler (&priv->focus_on_grab_dismissed.unmanaging_handler_id,
+                          priv->focus_on_grab_dismissed.window);
+  priv->focus_on_grab_dismissed.window = NULL;
+}
+
+static void
+focus_on_grab_dismissed_unmanaging_cb (MetaWindow  *window,
+                                       MetaDisplay *display)
+{
+  MetaDisplayPrivate *priv = meta_display_get_instance_private (display);
+
+  g_return_if_fail (priv->focus_on_grab_dismissed.window == window);
+
+  g_clear_signal_handler (&priv->focus_on_grab_dismissed.unmanaging_handler_id,
+                          priv->focus_on_grab_dismissed.window);
+  priv->focus_on_grab_dismissed.window = NULL;
+}
+
+void
+meta_display_queue_focus (MetaDisplay *display,
+                          MetaWindow  *window)
+{
+  MetaDisplayPrivate *priv = meta_display_get_instance_private (display);
+
+  g_clear_signal_handler (&priv->focus_on_grab_dismissed.unmanaging_handler_id,
+                          priv->focus_on_grab_dismissed.window);
+
+  priv->focus_on_grab_dismissed.window = window;
+  priv->focus_on_grab_dismissed.unmanaging_handler_id =
+    g_signal_connect (window, "unmanaging",
+                      G_CALLBACK (focus_on_grab_dismissed_unmanaging_cb),
+                      display);
+}
+
 /**
  * meta_display_xserver_time_is_before:
  * @display: a #MetaDisplay
diff --git a/src/core/window.c b/src/core/window.c
index 9e1082585..dca30a1c5 100644
--- a/src/core/window.c
+++ b/src/core/window.c
@@ -1939,15 +1939,6 @@ window_state_on_map (MetaWindow *window,
       return;
     }
 
-  /* Do not focus window on map if input is already taken by the
-   * compositor.
-   */
-  if (!meta_display_windows_are_interactable (window->display))
-    {
-      *takes_focus = FALSE;
-      return;
-    }
-
   /* When strict focus mode is enabled, prevent new windows from taking
    * focus unless they are ancestors to the transient.
    */
@@ -2262,7 +2253,10 @@ meta_window_show (MetaWindow *window)
 
           timestamp = meta_display_get_current_time_roundtrip (window->display);
 
-          meta_window_focus (window, timestamp);
+          if (meta_display_windows_are_interactable (window->display))
+            meta_window_focus (window, timestamp);
+          else
+            meta_display_queue_focus (window->display, window);
         }
       else if (display->x11_display)
         {