diff --git a/public/app/features/alerting/unified/components/rules/RulesFilter.test.tsx b/public/app/features/alerting/unified/components/rules/RulesFilter.test.tsx
index 4f7b1877828..536a496b198 100644
--- a/public/app/features/alerting/unified/components/rules/RulesFilter.test.tsx
+++ b/public/app/features/alerting/unified/components/rules/RulesFilter.test.tsx
@@ -1,10 +1,13 @@
 import { render, screen } from '@testing-library/react';
 import userEvent from '@testing-library/user-event';
 import React from 'react';
+import { TestProvider } from 'test/helpers/TestProvider';
+import { byLabelText, byRole } from 'testing-library-selector';
 
-import { logInfo } from '@grafana/runtime';
+import { locationService, logInfo, setDataSourceSrv } from '@grafana/runtime';
 
 import { LogMessages } from '../../Analytics';
+import { MockDataSourceSrv } from '../../mocks';
 
 import RulesFilter from './RulesFilter';
 
@@ -13,23 +16,68 @@ jest.mock('@grafana/runtime', () => {
   return {
     ...original,
     logInfo: jest.fn(),
-    DataSourcePicker: () => <></>,
   };
 });
 
-jest.mock('react-router-dom', () => ({
-  useLocation: () => ({
-    pathname: 'localhost:3000/example/path',
-  }),
-}));
+setDataSourceSrv(new MockDataSourceSrv({}));
 
-jest.mock('../../utils/misc', () => ({
-  getFiltersFromUrlParams: jest.fn(() => ({ dataSource: {}, alertState: {}, queryString: '', ruleType: '' })),
-}));
+const ui = {
+  stateFilter: {
+    firing: byRole('radio', { name: 'Firing' }),
+    normal: byRole('radio', { name: 'Normal' }),
+  },
+  ruleType: {
+    alert: byRole('radio', { name: 'Alert' }),
+  },
+  health: {
+    ok: byRole('radio', { name: 'Ok' }),
+  },
+  searchInput: byLabelText('Search'),
+};
+
+beforeEach(() => {
+  locationService.replace({ search: '' });
+});
+
+describe('RulesFilter', () => {
+  it('Should apply state filter to the search input', async () => {
+    const user = userEvent.setup();
+
+    render(<RulesFilter />, { wrapper: TestProvider });
+
+    await user.click(ui.stateFilter.firing.get());
+
+    expect(ui.searchInput.get()).toHaveValue('state:firing');
+  });
+
+  it('Should apply multiple UI-based filters to the search input', async () => {
+    const user = userEvent.setup();
+
+    render(<RulesFilter />, { wrapper: TestProvider });
+
+    await user.click(ui.health.ok.get());
+    await user.click(ui.ruleType.alert.get());
+    await user.click(ui.stateFilter.normal.get());
+
+    expect(ui.searchInput.get()).toHaveValue('health:ok type:alerting state:inactive');
+  });
+
+  it('Should combine UI filters and typed expressions', async () => {
+    const user = userEvent.setup();
+
+    render(<RulesFilter />, { wrapper: TestProvider });
+
+    await user.type(ui.searchInput.get(), 'cpu{Enter}');
+    await user.click(ui.health.ok.get());
+    await user.type(ui.searchInput.get(), ' usage');
+
+    expect(ui.searchInput.get()).toHaveValue('cpu health:ok usage');
+  });
+});
 
 describe('Analytics', () => {
   it('Sends log info when clicking alert state filters', async () => {
-    render(<RulesFilter />);
+    render(<RulesFilter />, { wrapper: TestProvider });
 
     const button = screen.getByText('Pending');
 
diff --git a/public/app/features/alerting/unified/components/rules/RulesFilter.tsx b/public/app/features/alerting/unified/components/rules/RulesFilter.tsx
index e2ec4b7103c..829dfe6f5fa 100644
--- a/public/app/features/alerting/unified/components/rules/RulesFilter.tsx
+++ b/public/app/features/alerting/unified/components/rules/RulesFilter.tsx
@@ -1,5 +1,5 @@
 import { css } from '@emotion/css';
-import React, { useRef, useState } from 'react';
+import React, { useEffect, useRef, useState } from 'react';
 import { useForm } from 'react-hook-form';
 
 import { DataSourceInstanceSettings, GrafanaTheme2, SelectableValue } from '@grafana/data';
@@ -69,6 +69,14 @@ const RulesFilter = ({ onFilterCleared = () => undefined }: RulesFilerProps) =>
   const dataSourceKey = `dataSource-${filterKey}`;
   const queryStringKey = `queryString-${filterKey}`;
 
+  const searchQueryRef = useRef<HTMLInputElement | null>(null);
+  const { handleSubmit, register, setValue } = useForm<{ searchQuery: string }>({ defaultValues: { searchQuery } });
+  const { ref, ...rest } = register('searchQuery');
+
+  useEffect(() => {
+    setValue('searchQuery', searchQuery);
+  }, [searchQuery, setValue]);
+
   const handleDataSourceChange = (dataSourceValue: DataSourceInstanceSettings) => {
     updateFilters({ ...filterState, dataSourceName: dataSourceValue.name });
     setFilterKey((key) => key + 1);
@@ -106,10 +114,6 @@ const RulesFilter = ({ onFilterCleared = () => undefined }: RulesFilerProps) =>
     setTimeout(() => setFilterKey(filterKey + 1), 100);
   };
 
-  const searchQueryRef = useRef<HTMLInputElement | null>(null);
-  const { handleSubmit, register } = useForm<{ searchQuery: string }>({ defaultValues: { searchQuery } });
-  const { ref, ...rest } = register('searchQuery');
-
   const searchIcon = <Icon name={'search'} />;
   return (
     <div className={styles.container}>
@@ -158,7 +162,7 @@ const RulesFilter = ({ onFilterCleared = () => undefined }: RulesFilerProps) =>
             >
               <Field
                 label={
-                  <Label>
+                  <Label htmlFor="rulesSearchInput">
                     <Stack gap={0.5}>
                       <span>Search</span>
                       <HoverCard content={<SearchQueryHelp />}>
@@ -169,6 +173,7 @@ const RulesFilter = ({ onFilterCleared = () => undefined }: RulesFilerProps) =>
                 }
               >
                 <Input
+                  id="rulesSearchInput"
                   key={queryStringKey}
                   prefix={searchIcon}
                   ref={(e) => {