diff --git a/src/core/display.c b/src/core/display.c
index 9730d48f7..81df26337 100644
--- a/src/core/display.c
+++ b/src/core/display.c
@@ -941,9 +941,6 @@ meta_display_new (MetaContext  *context,
   MetaDisplay *display;
   MetaDisplayPrivate *priv;
   guint32 timestamp;
-#ifdef HAVE_X11_CLIENT
-  Window old_active_xwindow = None;
-#endif
   MetaMonitorManager *monitor_manager;
   MetaSettings *settings;
   MetaInputCapture *input_capture;
@@ -1059,14 +1056,6 @@ meta_display_new (MetaContext  *context,
   display->last_focus_time = timestamp;
   display->last_user_time = timestamp;
 
-#ifdef HAVE_X11
-  if (!meta_is_wayland_compositor ())
-    meta_prop_get_window (display->x11_display,
-                          display->x11_display->xroot,
-                          display->x11_display->atom__NET_ACTIVE_WINDOW,
-                          &old_active_xwindow);
-#endif
-
   if (!meta_compositor_manage (display->compositor, error))
     {
       g_object_unref (display);
@@ -1087,30 +1076,7 @@ meta_display_new (MetaContext  *context,
   g_signal_connect (display->gesture_tracker, "state-changed",
                     G_CALLBACK (gesture_tracker_state_changed), display);
 
-  /* We know that if mutter is running as a Wayland compositor,
-   * we start out with no windows.
-   */
-#ifdef HAVE_X11_CLIENT
-  if (!meta_is_wayland_compositor ())
-    meta_display_manage_all_xwindows (display);
-
-  if (old_active_xwindow != None)
-    {
-      MetaWindow *old_active_window;
-      old_active_window = meta_x11_display_lookup_x_window (display->x11_display,
-                                                            old_active_xwindow);
-      if (old_active_window)
-        meta_window_focus (old_active_window, timestamp);
-      else
-        meta_display_unset_input_focus (display, timestamp);
-    }
-  else
-    {
-      meta_display_unset_input_focus (display, timestamp);
-    }
-#else
   meta_display_unset_input_focus (display, timestamp);
-#endif
 
   g_signal_connect (stage, "notify::is-grabbed",
                     G_CALLBACK (on_is_grabbed_changed), display);
diff --git a/src/x11/meta-x11-display.c b/src/x11/meta-x11-display.c
index 0ad52b9a0..65eb217aa 100644
--- a/src/x11/meta-x11-display.c
+++ b/src/x11/meta-x11-display.c
@@ -306,7 +306,32 @@ static void
 on_x11_display_opened (MetaX11Display *x11_display,
                        MetaDisplay    *display)
 {
+  Window old_active_xwindow = None;
+
+  if (!meta_is_wayland_compositor ())
+    {
+      meta_prop_get_window (display->x11_display,
+                            display->x11_display->xroot,
+                            display->x11_display->atom__NET_ACTIVE_WINDOW,
+                            &old_active_xwindow);
+    }
+
   meta_display_manage_all_xwindows (display);
+
+  if (old_active_xwindow != None)
+    {
+      MetaWindow *old_active_window;
+
+      old_active_window = meta_x11_display_lookup_x_window (x11_display,
+                                                            old_active_xwindow);
+      if (old_active_window)
+        {
+          uint32_t timestamp;
+
+          timestamp = display->x11_display->timestamp;
+          meta_window_focus (old_active_window, timestamp);
+        }
+    }
 }
 
 static void