diff --git a/public/app/app.ts b/public/app/app.ts
index 88f85dee5a0..97bff0eb9cc 100644
--- a/public/app/app.ts
+++ b/public/app/app.ts
@@ -82,6 +82,7 @@ import { preloadPlugins } from './features/plugins/pluginPreloader';
 import { QueryRunner } from './features/query/state/QueryRunner';
 import { runRequest } from './features/query/state/runRequest';
 import { initWindowRuntime } from './features/runtime/init';
+import { cleanupOldExpandedFolders } from './features/search/utils';
 import { variableAdapters } from './features/variables/adapters';
 import { createAdHocVariableAdapter } from './features/variables/adhoc/adapter';
 import { createConstantVariableAdapter } from './features/variables/constant/adapter';
@@ -215,6 +216,13 @@ export class GrafanaApp {
       // Read initial kiosk mode from url at app startup
       chromeService.setKioskModeFromUrl(queryParams.kiosk);
 
+      // Clean up old search local storage values
+      try {
+        cleanupOldExpandedFolders();
+      } catch (err) {
+        console.warn('Failed to clean up old expanded folders', err);
+      }
+
       this.context = {
         backend: backendSrv,
         location: locationService,
diff --git a/public/app/features/search/constants.ts b/public/app/features/search/constants.ts
index 2580147cf36..8b66939e15d 100644
--- a/public/app/features/search/constants.ts
+++ b/public/app/features/search/constants.ts
@@ -6,6 +6,7 @@ export const SEARCH_ITEM_HEIGHT = 58;
 export const SEARCH_ITEM_MARGIN = 8;
 export const DEFAULT_SORT = { label: 'A\u2013Z', value: 'alpha-asc' };
 export const SECTION_STORAGE_KEY = 'search.sections';
+export const SEARCH_EXPANDED_FOLDER_STORAGE_KEY = 'grafana.search.expanded-folder';
 export const GENERAL_FOLDER_ID = 0;
 export const GENERAL_FOLDER_UID = 'general';
 export const GENERAL_FOLDER_TITLE = 'General';
diff --git a/public/app/features/search/page/components/FolderSection.tsx b/public/app/features/search/page/components/FolderSection.tsx
index 55dbf0aaa8b..9f3ea0b8d17 100644
--- a/public/app/features/search/page/components/FolderSection.tsx
+++ b/public/app/features/search/page/components/FolderSection.tsx
@@ -1,16 +1,15 @@
 import { css } from '@emotion/css';
-import React, { useCallback, useId } from 'react';
-import { useAsync, useLocalStorage } from 'react-use';
+import React, { useCallback, useId, useState } from 'react';
+import { useAsync } from 'react-use';
 
 import { GrafanaTheme2, toIconName } from '@grafana/data';
 import { selectors } from '@grafana/e2e-selectors';
 import { Card, Checkbox, CollapsableSection, Icon, Spinner, useStyles2 } from '@grafana/ui';
 import { config } from 'app/core/config';
 import { t } from 'app/core/internationalization';
-import { getSectionStorageKey } from 'app/features/search/utils';
 
 import { SearchItem } from '../..';
-import { GENERAL_FOLDER_UID } from '../../constants';
+import { GENERAL_FOLDER_UID, SEARCH_EXPANDED_FOLDER_STORAGE_KEY } from '../../constants';
 import { getGrafanaSearcher } from '../../service';
 import { getFolderChildren } from '../../service/folders';
 import { queryResultToViewItem } from '../../service/utils';
@@ -57,9 +56,14 @@ export const FolderSection = ({
   renderStandaloneBody,
   tags,
 }: SectionHeaderProps) => {
+  const uid = section.uid;
   const editable = selectionToggle != null;
+
   const styles = useStyles2(useCallback((theme: GrafanaTheme2) => getSectionHeaderStyles(theme, editable), [editable]));
-  const [sectionExpanded, setSectionExpanded] = useLocalStorage(getSectionStorageKey(section.title), false);
+  const [sectionExpanded, setSectionExpanded] = useState(() => {
+    const lastExpandedFolder = window.localStorage.getItem(SEARCH_EXPANDED_FOLDER_STORAGE_KEY);
+    return lastExpandedFolder === uid;
+  });
 
   const results = useAsync(async () => {
     if (!sectionExpanded && !renderStandaloneBody) {
@@ -72,7 +76,20 @@ export const FolderSection = ({
   }, [sectionExpanded, tags]);
 
   const onSectionExpand = () => {
-    setSectionExpanded(!sectionExpanded);
+    const newExpandedValue = !sectionExpanded;
+
+    if (newExpandedValue) {
+      // If we've just expanded the section, remember it to local storage
+      window.localStorage.setItem(SEARCH_EXPANDED_FOLDER_STORAGE_KEY, uid);
+    } else {
+      // Else, when closing a section, remove it from local storage only if this folder was the most recently opened
+      const lastExpandedFolder = window.localStorage.getItem(SEARCH_EXPANDED_FOLDER_STORAGE_KEY);
+      if (lastExpandedFolder === uid) {
+        window.localStorage.removeItem(SEARCH_EXPANDED_FOLDER_STORAGE_KEY);
+      }
+    }
+
+    setSectionExpanded(newExpandedValue);
   };
 
   const onToggleFolder = (evt: React.FormEvent) => {
diff --git a/public/app/features/search/utils.ts b/public/app/features/search/utils.ts
index 7c942ec1174..c93ec642ed8 100644
--- a/public/app/features/search/utils.ts
+++ b/public/app/features/search/utils.ts
@@ -14,6 +14,18 @@ export const hasFilters = (query: SearchState) => {
   return Boolean(query.query || query.tag?.length > 0 || query.starred || query.sort);
 };
 
+/** Cleans up old local storage values that remembered many open folders */
+export const cleanupOldExpandedFolders = () => {
+  const keyPrefix = SECTION_STORAGE_KEY + '.';
+
+  for (let index = 0; index < window.localStorage.length; index++) {
+    const lsKey = window.localStorage.key(index);
+    if (lsKey?.startsWith(keyPrefix)) {
+      window.localStorage.removeItem(lsKey);
+    }
+  }
+};
+
 /**
  * Get storage key for a dashboard folder by its title
  * @param title