diff --git a/gtk/gtkpopover.c b/gtk/gtkpopover.c
index bdb8c6aaf0..65e1b05841 100644
--- a/gtk/gtkpopover.c
+++ b/gtk/gtkpopover.c
@@ -1455,7 +1455,7 @@ _gtk_popover_parent_size_allocate (GtkWidget     *widget,
 static void
 _unmanage_popover (GObject *object)
 {
-  g_object_run_dispose (object);
+  gtk_popover_update_relative_to (GTK_POPOVER (object), NULL);
   g_object_unref (object);
 }
 
@@ -1577,6 +1577,8 @@ gtk_popover_update_relative_to (GtkPopover *popover,
       priv->window = NULL;
     }
 
+  g_clear_object (&priv->prev_focus_widget);
+
   if (priv->widget)
     {
       if (g_signal_handler_is_connected (priv->widget, priv->hierarchy_changed_id))