diff --git a/src/core/events.c b/src/core/events.c
index 1767dded3..2a3f04ba9 100644
--- a/src/core/events.c
+++ b/src/core/events.c
@@ -34,6 +34,7 @@
 #include "core/display-private.h"
 #include "core/window-private.h"
 #include "meta/meta-backend.h"
+#include "x11/meta-x11-display-private.h"
 
 #ifdef HAVE_NATIVE_BACKEND
 #include "backends/native/meta-backend-native.h"
@@ -241,6 +242,9 @@ meta_display_handle_event (MetaDisplay        *display,
           display->grabbed_in_clutter = FALSE;
           meta_compositor_grab_end (compositor);
         }
+
+      if (display->x11_display)
+        meta_x11_display_sync_input_focus (display->x11_display);
     }
 
   device = clutter_event_get_device (event);
diff --git a/src/x11/meta-x11-display-private.h b/src/x11/meta-x11-display-private.h
index 798b9ab30..a4e4b07e3 100644
--- a/src/x11/meta-x11-display-private.h
+++ b/src/x11/meta-x11-display-private.h
@@ -278,6 +278,8 @@ void meta_x11_display_set_input_focus (MetaX11Display *x11_display,
                                        gboolean        focus_frame,
                                        uint32_t        timestamp);
 
+void meta_x11_display_sync_input_focus (MetaX11Display *x11_display);
+
 MetaDisplay * meta_x11_display_get_display (MetaX11Display *x11_display);
 
 #endif /* META_X11_DISPLAY_PRIVATE_H */
diff --git a/src/x11/meta-x11-display.c b/src/x11/meta-x11-display.c
index 33d9ad5cb..16b564d55 100644
--- a/src/x11/meta-x11-display.c
+++ b/src/x11/meta-x11-display.c
@@ -2011,6 +2011,10 @@ meta_x11_display_set_input_focus_internal (MetaX11Display *x11_display,
                                            Window          xwindow,
                                            uint32_t        timestamp)
 {
+  if (xwindow != None &&
+      !meta_display_windows_are_interactable (x11_display->display))
+    return;
+
   meta_x11_error_trap_push (x11_display);
 
   /* In order for mutter to know that the focus request succeeded, we track
@@ -2083,6 +2087,22 @@ meta_x11_display_set_input_focus_xwindow (MetaX11Display *x11_display,
   x11_display->display->last_focus_time = timestamp;
 }
 
+void
+meta_x11_display_sync_input_focus (MetaX11Display *x11_display)
+{
+  guint timestamp;
+
+  if (!meta_display_windows_are_interactable (x11_display->display))
+    return;
+
+  meta_x11_error_trap_push (x11_display);
+  timestamp = meta_display_get_current_time (x11_display->display);
+  meta_x11_display_set_input_focus_internal (x11_display,
+                                             x11_display->focus_xwindow,
+                                             timestamp);
+  meta_x11_error_trap_pop (x11_display);
+}
+
 static MetaX11DisplayLogicalMonitorData *
 get_x11_display_logical_monitor_data (MetaLogicalMonitor *logical_monitor)
 {