diff --git a/doc/classes/EditorInspector.xml b/doc/classes/EditorInspector.xml
index cfdc172fd1d..6b25be490ed 100644
--- a/doc/classes/EditorInspector.xml
+++ b/doc/classes/EditorInspector.xml
@@ -28,6 +28,7 @@
 		</method>
 	</methods>
 	<members>
+		<member name="follow_focus" type="bool" setter="set_follow_focus" getter="is_following_focus" overrides="ScrollContainer" default="true" />
 		<member name="horizontal_scroll_mode" type="int" setter="set_horizontal_scroll_mode" getter="get_horizontal_scroll_mode" overrides="ScrollContainer" enum="ScrollContainer.ScrollMode" default="0" />
 	</members>
 	<signals>
diff --git a/editor/editor_inspector.cpp b/editor/editor_inspector.cpp
index 1e5acce0329..7eb0732dbb6 100644
--- a/editor/editor_inspector.cpp
+++ b/editor/editor_inspector.cpp
@@ -2766,8 +2766,9 @@ void EditorInspector::update_tree() {
 	// TODO: Can be useful to store more context for the focusable, such as the caret position in LineEdit.
 	StringName current_selected = property_selected;
 	int current_focusable = -1;
-	// Temporarily disable focus following to avoid jumping while the inspector is updating.
-	set_follow_focus(false);
+
+	// Temporarily disable focus following on the root inspector to avoid jumping while the inspector is updating.
+	get_root_inspector()->set_follow_focus(false);
 
 	if (property_focusable != -1) {
 		// Check that focusable is actually focusable.
@@ -2795,6 +2796,7 @@ void EditorInspector::update_tree() {
 	_clear(!object);
 
 	if (!object) {
+		get_root_inspector()->set_follow_focus(true);
 		return;
 	}
 
@@ -3532,7 +3534,8 @@ void EditorInspector::update_tree() {
 		// Updating inspector might invalidate some editing owners.
 		EditorNode::get_singleton()->hide_unused_editors();
 	}
-	set_follow_focus(true);
+
+	get_root_inspector()->set_follow_focus(true);
 }
 
 void EditorInspector::update_property(const String &p_prop) {
@@ -3777,11 +3780,10 @@ void EditorInspector::set_use_wide_editors(bool p_enable) {
 	wide_editors = p_enable;
 }
 
-void EditorInspector::set_sub_inspector(bool p_enable) {
-	sub_inspector = p_enable;
-	if (!is_inside_tree()) {
-		return;
-	}
+void EditorInspector::set_root_inspector(EditorInspector *p_root_inspector) {
+	root_inspector = p_root_inspector;
+	// Only the root inspector should follow focus.
+	set_follow_focus(false);
 }
 
 void EditorInspector::set_use_deletable_properties(bool p_enabled) {
@@ -4099,13 +4101,13 @@ void EditorInspector::_notification(int p_what) {
 			EditorFeatureProfileManager::get_singleton()->connect("current_feature_profile_changed", callable_mp(this, &EditorInspector::_feature_profile_changed));
 			set_process(is_visible_in_tree());
 			add_theme_style_override(SceneStringName(panel), get_theme_stylebox(SceneStringName(panel), SNAME("Tree")));
-			if (!sub_inspector) {
+			if (!is_sub_inspector()) {
 				get_tree()->connect("node_removed", callable_mp(this, &EditorInspector::_node_removed));
 			}
 		} break;
 
 		case NOTIFICATION_PREDELETE: {
-			if (!sub_inspector && is_inside_tree()) {
+			if (!is_sub_inspector() && is_inside_tree()) {
 				get_tree()->disconnect("node_removed", callable_mp(this, &EditorInspector::_node_removed));
 			}
 			edit(nullptr);
@@ -4164,7 +4166,7 @@ void EditorInspector::_notification(int p_what) {
 
 		case EditorSettings::NOTIFICATION_EDITOR_SETTINGS_CHANGED: {
 			bool needs_update = false;
-			if (EditorThemeManager::is_generated_theme_outdated() && !sub_inspector) {
+			if (!is_sub_inspector() && EditorThemeManager::is_generated_theme_outdated()) {
 				add_theme_style_override(SceneStringName(panel), get_theme_stylebox(SceneStringName(panel), SNAME("Tree")));
 			}
 
diff --git a/editor/editor_inspector.h b/editor/editor_inspector.h
index 29ee2348832..7d64d217dcc 100644
--- a/editor/editor_inspector.h
+++ b/editor/editor_inspector.h
@@ -486,6 +486,7 @@ class EditorInspector : public ScrollContainer {
 	static Ref<EditorInspectorPlugin> inspector_plugins[MAX_PLUGINS];
 	static int inspector_plugin_count;
 
+	EditorInspector *root_inspector = nullptr;
 	VBoxContainer *main_vbox = nullptr;
 
 	// Map used to cache the instantiated editors.
@@ -514,7 +515,6 @@ class EditorInspector : public ScrollContainer {
 	bool update_all_pending = false;
 	bool read_only = false;
 	bool keying = false;
-	bool sub_inspector = false;
 	bool wide_editors = false;
 	bool deletable_properties = false;
 
@@ -645,8 +645,9 @@ public:
 	String get_object_class() const;
 
 	void set_use_wide_editors(bool p_enable);
-	void set_sub_inspector(bool p_enable);
-	bool is_sub_inspector() const { return sub_inspector; }
+	void set_root_inspector(EditorInspector *p_root_inspector);
+	EditorInspector *get_root_inspector() { return is_sub_inspector() ? root_inspector : this; }
+	bool is_sub_inspector() const { return root_inspector != nullptr; }
 
 	void set_use_deletable_properties(bool p_enabled);
 
diff --git a/editor/editor_properties.cpp b/editor/editor_properties.cpp
index 19a4165041d..b6026be0717 100644
--- a/editor/editor_properties.cpp
+++ b/editor/editor_properties.cpp
@@ -3238,7 +3238,10 @@ void EditorPropertyResource::update_property() {
 				sub_inspector->set_vertical_scroll_mode(ScrollContainer::SCROLL_MODE_DISABLED);
 				sub_inspector->set_use_doc_hints(true);
 
-				sub_inspector->set_sub_inspector(true);
+				EditorInspector *parent_inspector = get_parent_inspector();
+				ERR_FAIL_NULL(parent_inspector);
+				sub_inspector->set_root_inspector(parent_inspector->get_root_inspector());
+
 				sub_inspector->set_property_name_style(InspectorDock::get_singleton()->get_property_name_style());
 
 				sub_inspector->connect("property_keyed", callable_mp(this, &EditorPropertyResource::_sub_inspector_property_keyed));
diff --git a/editor/inspector_dock.cpp b/editor/inspector_dock.cpp
index dc07403213c..e175ad9cbcd 100644
--- a/editor/inspector_dock.cpp
+++ b/editor/inspector_dock.cpp
@@ -799,7 +799,7 @@ InspectorDock::InspectorDock(EditorData &p_editor_data) {
 	inspector->set_use_folding(!bool(EDITOR_GET("interface/inspector/disable_folding")));
 	inspector->register_text_enter(search);
 
-	inspector->set_use_filter(true); // TODO: check me
+	inspector->set_use_filter(true);
 
 	inspector->connect("resource_selected", callable_mp(this, &InspectorDock::_resource_selected));