diff --git a/public/app/features/alerting/unified/api/prometheusApi.ts b/public/app/features/alerting/unified/api/prometheusApi.ts
index d4a23770b01..a64f87296f2 100644
--- a/public/app/features/alerting/unified/api/prometheusApi.ts
+++ b/public/app/features/alerting/unified/api/prometheusApi.ts
@@ -95,6 +95,7 @@ export const prometheusApi = alertingApi.injectEndpoints({
         limitAlerts,
         groupNextToken,
         title,
+        dashboardUid,
       }) => ({
         url: `api/prometheus/grafana/api/v1/rules`,
         params: {
@@ -109,6 +110,7 @@ export const prometheusApi = alertingApi.injectEndpoints({
           group_limit: groupLimit?.toFixed(0),
           group_next_token: groupNextToken,
           'search.rule_name': title,
+          dashboard_uid: dashboardUid,
         },
       }),
       providesTags: (_result, _error, { folderUid, groupName, ruleName }) => {
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 cdd4bb2544e..e7a357c8498 100644
--- a/public/app/features/alerting/unified/rule-list/hooks/prometheusGroupsGenerator.ts
+++ b/public/app/features/alerting/unified/rule-list/hooks/prometheusGroupsGenerator.ts
@@ -48,6 +48,7 @@ interface GrafanaPromApiFilter {
   contactPoint?: string;
   title?: string;
   type?: 'alerting' | 'recording';
+  dashboardUid?: string;
 }
 
 interface GrafanaFetchGroupsOptions extends FetchGroupsOptions {
diff --git a/public/app/features/alerting/unified/rule-list/hooks/useFilteredRulesIterator.test.ts b/public/app/features/alerting/unified/rule-list/hooks/useFilteredRulesIterator.test.ts
index 298ec747f56..9f597922867 100644
--- a/public/app/features/alerting/unified/rule-list/hooks/useFilteredRulesIterator.test.ts
+++ b/public/app/features/alerting/unified/rule-list/hooks/useFilteredRulesIterator.test.ts
@@ -22,17 +22,17 @@ describe('hasClientSideFilters', () => {
       config.featureToggles.alertingUIUseBackendFilters = true;
     });
 
-    it('should return false for backend-supported filters (title and type)', () => {
+    it('should return false for backend-supported filters', () => {
       expect(hasClientSideFilters(getFilter({ freeFormWords: ['cpu'] }))).toBe(false);
       expect(hasClientSideFilters(getFilter({ ruleName: 'test' }))).toBe(false);
       expect(hasClientSideFilters(getFilter({ ruleType: PromRuleType.Alerting }))).toBe(false);
+      expect(hasClientSideFilters(getFilter({ dashboardUid: 'test-dashboard' }))).toBe(false);
     });
 
     it('should return true for client-side only filters', () => {
       expect(hasClientSideFilters(getFilter({ namespace: 'test' }))).toBe(true);
       expect(hasClientSideFilters(getFilter({ dataSourceNames: ['prometheus'] }))).toBe(true);
       expect(hasClientSideFilters(getFilter({ labels: ['severity=critical'] }))).toBe(true);
-      expect(hasClientSideFilters(getFilter({ dashboardUid: 'test-dashboard' }))).toBe(true);
       expect(hasClientSideFilters(getFilter({ ruleSource: RuleSource.DataSource }))).toBe(true);
     });
 
@@ -46,10 +46,11 @@ describe('hasClientSideFilters', () => {
       config.featureToggles.alertingUIUseBackendFilters = false;
     });
 
-    it('should return true for title and type filters (client-side fallback)', () => {
+    it('should return true for backend-supported filters when backend filtering is disabled', () => {
       expect(hasClientSideFilters(getFilter({ freeFormWords: ['cpu'] }))).toBe(true);
       expect(hasClientSideFilters(getFilter({ ruleName: 'test' }))).toBe(true);
       expect(hasClientSideFilters(getFilter({ ruleType: PromRuleType.Alerting }))).toBe(true);
+      expect(hasClientSideFilters(getFilter({ dashboardUid: 'test-dashboard' }))).toBe(true);
     });
 
     it('should return true for client-side only filters', () => {
@@ -70,11 +71,12 @@ describe('hasClientSideFilters', () => {
       config.featureToggles.alertingUIUseBackendFilters = undefined;
     });
 
-    it('should return true for title and type filters (backward compatibility)', () => {
+    it('should default to client-side filtering for backward compatibility', () => {
       // Default behavior should be client-side filtering
       expect(hasClientSideFilters(getFilter({ freeFormWords: ['cpu'] }))).toBe(true);
       expect(hasClientSideFilters(getFilter({ ruleName: 'test' }))).toBe(true);
       expect(hasClientSideFilters(getFilter({ ruleType: PromRuleType.Alerting }))).toBe(true);
+      expect(hasClientSideFilters(getFilter({ dashboardUid: 'test-dashboard' }))).toBe(true);
     });
   });
 });
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 3e225ed9b7a..d2a577a1d23 100644
--- a/public/app/features/alerting/unified/rule-list/hooks/useFilteredRulesIterator.ts
+++ b/public/app/features/alerting/unified/rule-list/hooks/useFilteredRulesIterator.ts
@@ -84,6 +84,7 @@ export function useFilteredRulesIteratorProvider() {
 
     const titleSearch = useBackendFilters ? buildTitleSearch(filterState) : undefined;
     const ruleType = useBackendFilters ? filterState.ruleType : undefined;
+    const dashboardUid = useBackendFilters ? filterState.dashboardUid : undefined;
 
     const grafanaRulesGenerator: AsyncIterableX<RuleWithOrigin> = from(
       grafanaGroupsGenerator(groupLimit, {
@@ -92,6 +93,7 @@ export function useFilteredRulesIteratorProvider() {
         state: filterState.ruleState ? [filterState.ruleState] : [],
         title: titleSearch,
         type: ruleType,
+        dashboardUid,
       })
     ).pipe(
       withAbort(abortController.signal),
@@ -160,14 +162,16 @@ export function hasClientSideFilters(filterState: RulesFilter): boolean {
   const useBackendFilters = shouldUseBackendFilters();
 
   return (
-    // When backend filters are disabled, title search and type filter need client-side filtering
+    // When backend filters are disabled, title search, type filter, and dashboard filter need client-side filtering
     (!useBackendFilters &&
-      (filterState.freeFormWords.length > 0 || Boolean(filterState.ruleName) || Boolean(filterState.ruleType))) ||
+      (filterState.freeFormWords.length > 0 ||
+        Boolean(filterState.ruleName) ||
+        Boolean(filterState.ruleType) ||
+        Boolean(filterState.dashboardUid))) ||
     // Client-side only filters:
     Boolean(filterState.namespace) ||
     filterState.dataSourceNames.length > 0 ||
     filterState.labels.length > 0 ||
-    Boolean(filterState.dashboardUid) ||
     filterState.ruleSource === RuleSource.DataSource
   );
 }