diff --git a/public/app/features/alerting/unified/api/prometheusApi.ts b/public/app/features/alerting/unified/api/prometheusApi.ts
index 8fce82f8755..01e5fdaa1b9 100644
--- a/public/app/features/alerting/unified/api/prometheusApi.ts
+++ b/public/app/features/alerting/unified/api/prometheusApi.ts
@@ -118,18 +118,20 @@ export const prometheusApi = alertingApi.injectEndpoints({
 export function usePopulateGrafanaPrometheusApiCache() {
   const dispatch = useDispatch();
 
-  const populateGroupResponseCache = useCallback(
-    (group: GrafanaPromRuleGroupDTO) => {
+  const populateGroupsResponseCache = useCallback(
+    (groups: GrafanaPromRuleGroupDTO[]) => {
       dispatch(
-        prometheusApi.util.upsertQueryData(
-          'getGrafanaGroups',
-          { folderUid: group.folderUid, groupName: group.name },
-          { data: { groups: [group] }, status: 'success' }
+        prometheusApi.util.upsertQueryEntries(
+          groups.map((group) => ({
+            endpointName: 'getGrafanaGroups',
+            arg: { folderUid: group.folderUid, groupName: group.name, limitAlerts: 0 },
+            value: { data: { groups: [group] }, status: 'success' },
+          }))
         )
       );
     },
     [dispatch]
   );
 
-  return { populateGroupResponseCache };
+  return { populateGroupsResponseCache };
 }
diff --git a/public/app/features/alerting/unified/rule-list/PaginatedDataSourceLoader.tsx b/public/app/features/alerting/unified/rule-list/PaginatedDataSourceLoader.tsx
index ec3fe298a91..76fc0c6bbec 100644
--- a/public/app/features/alerting/unified/rule-list/PaginatedDataSourceLoader.tsx
+++ b/public/app/features/alerting/unified/rule-list/PaginatedDataSourceLoader.tsx
@@ -51,9 +51,7 @@ function PaginatedGroupsLoader({ rulesSourceIdentifier, application, groupFilter
   const hasFilters = Boolean(groupFilter || namespaceFilter);
 
   const { uid, name } = rulesSourceIdentifier;
-  const prometheusGroupsGenerator = usePrometheusGroupsGenerator({
-    populateCache: hasFilters ? false : true,
-  });
+  const prometheusGroupsGenerator = usePrometheusGroupsGenerator();
 
   // If there are no filters we can match one frontend page to one API page.
   // However, if there are filters, we need to fetch more groups from the API to populate one frontend page
diff --git a/public/app/features/alerting/unified/rule-list/hooks/prometheusGroupsGenerator.ts b/public/app/features/alerting/unified/rule-list/hooks/prometheusGroupsGenerator.ts
index 184489ccdc2..71ee5537465 100644
--- a/public/app/features/alerting/unified/rule-list/hooks/prometheusGroupsGenerator.ts
+++ b/public/app/features/alerting/unified/rule-list/hooks/prometheusGroupsGenerator.ts
@@ -1,10 +1,9 @@
 import { useCallback } from 'react';
 
-import { useDispatch } from 'app/types/store';
 import { DataSourceRulesSourceIdentifier, RuleHealth } from 'app/types/unified-alerting';
 import { PromAlertingRuleState, PromRuleGroupDTO } from 'app/types/unified-alerting-dto';
 
-import { PromRulesResponse, prometheusApi } from '../../api/prometheusApi';
+import { PromRulesResponse, prometheusApi, usePopulateGrafanaPrometheusApiCache } from '../../api/prometheusApi';
 
 const { useLazyGetGroupsQuery, useLazyGetGrafanaGroupsQuery } = prometheusApi;
 
@@ -22,8 +21,7 @@ interface FetchGroupsOptions {
   groupNextToken?: string;
 }
 
-export function usePrometheusGroupsGenerator(hookOptions: UseGeneratorHookOptions = {}) {
-  const dispatch = useDispatch();
+export function usePrometheusGroupsGenerator() {
   const [getGroups] = useLazyGetGroupsQuery();
 
   return useCallback(
@@ -35,24 +33,12 @@ export function usePrometheusGroupsGenerator(hookOptions: UseGeneratorHookOption
           ...fetchOptions,
         }).unwrap();
 
-        if (hookOptions.populateCache) {
-          response.data.groups.forEach((group) => {
-            dispatch(
-              prometheusApi.util.upsertQueryData(
-                'getGroups',
-                { ruleSource: { uid: ruleSource.uid }, namespace: group.file, groupName: group.name },
-                { data: { groups: [group] }, status: 'success' }
-              )
-            );
-          });
-        }
-
         return response;
       };
 
       yield* genericGroupsGenerator(getRuleSourceGroupsWithCache, groupLimit);
     },
-    [getGroups, dispatch, hookOptions.populateCache]
+    [getGroups]
   );
 }
 
@@ -67,8 +53,8 @@ interface GrafanaFetchGroupsOptions extends FetchGroupsOptions {
 }
 
 export function useGrafanaGroupsGenerator(hookOptions: UseGeneratorHookOptions = {}) {
-  const dispatch = useDispatch();
   const [getGrafanaGroups] = useLazyGetGrafanaGroupsQuery();
+  const { populateGroupsResponseCache } = usePopulateGrafanaPrometheusApiCache();
 
   const getGroupsAndProvideCache = useCallback(
     async (fetchOptions: GrafanaFetchGroupsOptions) => {
@@ -78,25 +64,13 @@ export function useGrafanaGroupsGenerator(hookOptions: UseGeneratorHookOptions =
         ...fetchOptions.filter,
       }).unwrap();
 
-      // This is not mandatory to preload ruler rules, but it improves the UX
-      // Because the user waits a bit longer for the initial load but doesn't need to wait for each group to be loaded
       if (hookOptions.populateCache) {
-        const cacheAndRulerPreload = response.data.groups.map(async (group) => {
-          await dispatch(
-            prometheusApi.util.upsertQueryData(
-              'getGrafanaGroups',
-              { folderUid: group.folderUid, groupName: group.name, limitAlerts: hookOptions.limitAlerts },
-              { data: { groups: [group] }, status: 'success' }
-            )
-          );
-        });
-
-        await Promise.allSettled(cacheAndRulerPreload);
+        populateGroupsResponseCache(response.data.groups);
       }
 
       return response;
     },
-    [getGrafanaGroups, dispatch, hookOptions.populateCache, hookOptions.limitAlerts]
+    [getGrafanaGroups, hookOptions.limitAlerts, hookOptions.populateCache, populateGroupsResponseCache]
   );
 
   return useCallback(
diff --git a/public/app/features/alerting/unified/rule-list/hooks/useFilteredRulesIterator.ts b/public/app/features/alerting/unified/rule-list/hooks/useFilteredRulesIterator.ts
index 73095e0acff..216d59c10a7 100644
--- a/public/app/features/alerting/unified/rule-list/hooks/useFilteredRulesIterator.ts
+++ b/public/app/features/alerting/unified/rule-list/hooks/useFilteredRulesIterator.ts
@@ -15,7 +15,6 @@ import {
   PromRuleGroupDTO,
 } from 'app/types/unified-alerting-dto';
 
-import { usePopulateGrafanaPrometheusApiCache } from '../../api/prometheusApi';
 import { RulesFilter } from '../../search/rulesSearchParser';
 import {
   getDataSourceByUid,
@@ -52,7 +51,6 @@ interface GetIteratorResult {
 }
 
 export function useFilteredRulesIteratorProvider() {
-  const { populateGroupResponseCache } = usePopulateGrafanaPrometheusApiCache();
   const allExternalRulesSources = getExternalRulesSources();
 
   const prometheusGroupsGenerator = usePrometheusGroupsGenerator();
@@ -76,10 +74,7 @@ export function useFilteredRulesIteratorProvider() {
       concatMap((groups) =>
         groups
           .filter((group) => groupFilter(group, normalizedFilterState))
-          .flatMap((group) => {
-            populateGroupResponseCache(group);
-            return group.rules.map((rule) => [group, rule] as const);
-          })
+          .flatMap((group) => group.rules.map((rule) => [group, rule] as const))
           .filter(([, rule]) => ruleFilter(rule, normalizedFilterState))
           .map(([group, rule]) => mapGrafanaRuleToRuleWithOrigin(group, rule))
       ),