diff --git a/data/org.gnome.nautilus.gschema.xml b/data/org.gnome.nautilus.gschema.xml
index e32cac3e36d722d346abd8594fd301a958a4c323..cbc3290989c8c6c57dfc6dd58001911f856be44d 100644
--- a/data/org.gnome.nautilus.gschema.xml
+++ b/data/org.gnome.nautilus.gschema.xml
@@ -168,6 +168,11 @@
       <summary>Whether to show hidden files</summary>
       <description>This key is deprecated and ignored. The “show-hidden” key from “org.gtk.Settings.FileChooser” is now used instead.</description>
     </key>
+    <key type="b" name="migrated-gtk-settings">
+      <default>false</default>
+      <summary>Whether GTK 4 settings migration happened</summary>
+      <description>Whether settings shared with GtkFileChooser have been migrated from their GTK 3 key to the GTK 4 ones.</description>
+    </key>
     <key name="search-view" enum="org.gnome.nautilus.FolderView">
       <default>'list-view'</default>
       <summary>What viewer should be used when searching</summary>
diff --git a/src/nautilus-application.c b/src/nautilus-application.c
index c3e5881034bb6ff7ca6b3edc887b72710e9e4dfc..5d8d750b975581b905673aa6393de60447c4291c 100644
--- a/src/nautilus-application.c
+++ b/src/nautilus-application.c
@@ -1133,6 +1133,38 @@ icon_theme_changed_callback (GtkIconTheme *icon_theme,
     emit_change_signals_for_all_files_in_all_directories ();
 }
 
+static void
+maybe_migrate_gtk_filechooser_preferences (void)
+{
+    if (!g_settings_get_boolean (nautilus_preferences, NAUTILUS_PREFERENCES_MIGRATED_GTK_SETTINGS))
+    {
+        g_autoptr (GSettingsSchema) schema = NULL;
+
+        /* We don't depend on GTK 3. Check whether its schema is installed. */
+        schema = g_settings_schema_source_lookup (g_settings_schema_source_get_default (),
+                                                  "org.gtk.Settings.FileChooser",
+                                                  FALSE);
+        if (schema != NULL)
+        {
+            g_autoptr (GSettings) gtk3_settings = NULL;
+
+            gtk3_settings = g_settings_new_with_path ("org.gtk.Settings.FileChooser",
+                                                      "/org/gtk/settings/file-chooser/");
+            g_settings_set_boolean (gtk_filechooser_preferences,
+                                    NAUTILUS_PREFERENCES_SORT_DIRECTORIES_FIRST,
+                                    g_settings_get_boolean (gtk3_settings,
+                                                            NAUTILUS_PREFERENCES_SORT_DIRECTORIES_FIRST));
+            g_settings_set_boolean (gtk_filechooser_preferences,
+                                    NAUTILUS_PREFERENCES_SHOW_HIDDEN_FILES,
+                                    g_settings_get_boolean (gtk3_settings,
+                                                            NAUTILUS_PREFERENCES_SHOW_HIDDEN_FILES));
+        }
+        g_settings_set_boolean (nautilus_preferences,
+                                NAUTILUS_PREFERENCES_MIGRATED_GTK_SETTINGS,
+                                TRUE);
+    }
+}
+
 void
 nautilus_application_startup_common (NautilusApplication *self)
 {
@@ -1173,6 +1205,7 @@ nautilus_application_startup_common (NautilusApplication *self)
 
     if (g_strcmp0 (g_getenv ("RUNNING_TESTS"), "TRUE") != 0)
     {
+        maybe_migrate_gtk_filechooser_preferences ();
         nautilus_tag_manager_maybe_migrate_tracker2_data (priv->tag_manager);
     }
 
diff --git a/src/nautilus-global-preferences.c b/src/nautilus-global-preferences.c
index fd6d53e08194d359ff750f8a1825e9751c1341e9..6bc991908f2d767661987cab38997906b7e6aab7 100644
--- a/src/nautilus-global-preferences.c
+++ b/src/nautilus-global-preferences.c
@@ -59,8 +59,8 @@ nautilus_global_preferences_init (void)
     nautilus_icon_view_preferences = g_settings_new ("org.gnome.nautilus.icon-view");
     nautilus_list_view_preferences = g_settings_new ("org.gnome.nautilus.list-view");
     /* Some settings such as show hidden files are shared between Nautilus and GTK file chooser */
-    gtk_filechooser_preferences = g_settings_new_with_path ("org.gtk.Settings.FileChooser",
-                                                            "/org/gtk/settings/file-chooser/");
+    gtk_filechooser_preferences = g_settings_new_with_path ("org.gtk.gtk4.Settings.FileChooser",
+                                                            "/org/gtk/gtk4/settings/file-chooser/");
     gnome_lockdown_preferences = g_settings_new ("org.gnome.desktop.lockdown");
     gnome_interface_preferences = g_settings_new ("org.gnome.desktop.interface");
     gnome_privacy_preferences = g_settings_new ("org.gnome.desktop.privacy");
diff --git a/src/nautilus-global-preferences.h b/src/nautilus-global-preferences.h
index 5168f383fb06f4fa52094c2d6c63996c235019af..5a73717b3023f3dd90fdf1a80ba0f21c7bec3aeb 100644
--- a/src/nautilus-global-preferences.h
+++ b/src/nautilus-global-preferences.h
@@ -127,6 +127,9 @@ typedef enum
 /* Full Text Search enabled */
 #define NAUTILUS_PREFERENCES_FTS_ENABLED "fts-enabled"
 
+/* Gtk settings migration happened */
+#define NAUTILUS_PREFERENCES_MIGRATED_GTK_SETTINGS "migrated-gtk-settings"
+
 void nautilus_global_preferences_init                      (void);
 
 extern GSettings *nautilus_preferences;