diff --git a/editor/plugins/asset_library_editor_plugin.cpp b/editor/plugins/asset_library_editor_plugin.cpp
index 1345adc8ee6..904517b1192 100644
--- a/editor/plugins/asset_library_editor_plugin.cpp
+++ b/editor/plugins/asset_library_editor_plugin.cpp
@@ -557,8 +557,15 @@ void EditorAssetLibrary::_notification(int p_what) {
 			error_label->raise();
 		} break;
 		case NOTIFICATION_VISIBILITY_CHANGED: {
-			if (is_visible() && initial_loading) {
-				_repository_changed(0); // Update when shown for the first time.
+			if (is_visible()) {
+				// Focus the search box automatically when switching to the Templates tab (in the Project Manager)
+				// or switching to the AssetLib tab (in the editor).
+				// The Project Manager's project filter box is automatically focused in the project manager code.
+				filter->grab_focus();
+
+				if (initial_loading) {
+					_repository_changed(0); // Update when shown for the first time.
+				}
 			}
 		} break;
 		case NOTIFICATION_PROCESS: {
@@ -1332,6 +1339,11 @@ EditorAssetLibrary::EditorAssetLibrary(bool p_templates_only) {
 	library_main->add_theme_constant_override("separation", 10 * EDSCALE);
 
 	filter = memnew(LineEdit);
+	if (templates_only) {
+		filter->set_placeholder(TTR("Search templates, projects, and demos"));
+	} else {
+		filter->set_placeholder(TTR("Search assets (excluding templates, projects, and demos)"));
+	}
 	search_hb->add_child(filter);
 	filter->set_h_size_flags(Control::SIZE_EXPAND_FILL);
 	filter->connect("text_changed", callable_mp(this, &EditorAssetLibrary::_search_text_changed));
diff --git a/editor/project_manager.cpp b/editor/project_manager.cpp
index eda9499783a..1f5c14b6378 100644
--- a/editor/project_manager.cpp
+++ b/editor/project_manager.cpp
@@ -2331,6 +2331,17 @@ void ProjectManager::_on_order_option_changed(int p_idx) {
 	}
 }
 
+void ProjectManager::_on_tab_changed(int p_tab) {
+	if (p_tab == 0) { // Projects
+		// Automatically grab focus when the user moves from the Templates tab
+		// back to the Projects tab.
+		search_box->grab_focus();
+	}
+
+	// The Templates tab's search field is focused on display in the asset
+	// library editor plugin code.
+}
+
 void ProjectManager::_on_search_term_changed(const String &p_term) {
 	_project_list->set_search_term(p_term);
 	_project_list->sort_projects();
@@ -2456,6 +2467,7 @@ ProjectManager::ProjectManager() {
 	center_box->add_child(tabs);
 	tabs->set_anchors_and_offsets_preset(Control::PRESET_WIDE);
 	tabs->set_tab_align(TabContainer::ALIGN_LEFT);
+	tabs->connect("tab_changed", callable_mp(this, &ProjectManager::_on_tab_changed));
 
 	HBoxContainer *projects_hb = memnew(HBoxContainer);
 	projects_hb->set_name(TTR("Projects"));
@@ -2472,8 +2484,8 @@ ProjectManager::ProjectManager() {
 		search_tree_vb->add_child(hb);
 
 		search_box = memnew(LineEdit);
-		search_box->set_placeholder(TTR("Search"));
-		search_box->set_tooltip(TTR("The search box filters projects by name and last path component.\nTo filter projects by name and full path, the query must contain at least one `/` character."));
+		search_box->set_placeholder(TTR("Filter projects"));
+		search_box->set_tooltip(TTR("This field filters projects by name and last path component.\nTo filter projects by name and full path, the query must contain at least one `/` character."));
 		search_box->connect("text_changed", callable_mp(this, &ProjectManager::_on_search_term_changed));
 		search_box->set_h_size_flags(Control::SIZE_EXPAND_FILL);
 		hb->add_child(search_box);
diff --git a/editor/project_manager.h b/editor/project_manager.h
index 6dc0e67cba5..49d672a8e57 100644
--- a/editor/project_manager.h
+++ b/editor/project_manager.h
@@ -116,6 +116,7 @@ class ProjectManager : public Control {
 	void _files_dropped(PackedStringArray p_files, int p_screen);
 
 	void _on_order_option_changed(int p_idx);
+	void _on_tab_changed(int p_tab);
 	void _on_search_term_changed(const String &p_term);
 
 protected: