diff --git a/.github/CODEOWNERS b/.github/CODEOWNERS
index 7b81e1f23af..ff5a5950112 100644
--- a/.github/CODEOWNERS
+++ b/.github/CODEOWNERS
@@ -816,6 +816,7 @@ embed.go @grafana/grafana-as-code
 /.github/workflows/verify-kinds.yml @grafana/platform-monitoring
 /.github/workflows/dashboards-issue-add-label.yml @grafana/dashboards-squad
 /.github/workflows/run-schema-v2-e2e.yml  @grafana/dashboards-squad
+/.github/workflows/run-dashboard-search-e2e.yml  @grafana/grafana-search-and-storage
 /.github/workflows/ephemeral-instances-pr-comment.yml @grafana/grafana-backend-services-squad
 /.github/workflows/create-security-patch-from-security-mirror.yml @grafana/grafana-developer-enablement-squad
 /.github/workflows/core-plugins-build-and-release.yml @grafana/plugins-platform-frontend @grafana/plugins-platform-backend
diff --git a/.github/workflows/run-dashboard-search-e2e.yml b/.github/workflows/run-dashboard-search-e2e.yml
new file mode 100644
index 00000000000..aa41c96e0b7
--- /dev/null
+++ b/.github/workflows/run-dashboard-search-e2e.yml
@@ -0,0 +1,121 @@
+name: Run dashboard search e2e
+
+on:
+  push:
+    branches:
+      - main
+  pull_request:
+    branches:
+      - main
+
+env:
+  ARCH: linux-amd64
+
+jobs:
+  setup:
+    runs-on: ubuntu-latest
+    if: github.event.pull_request.draft == false
+    outputs:
+      ini_files: ${{ steps.get_files.outputs.ini_files }}
+
+    steps:
+      - name: Checkout
+        uses: actions/checkout@v4
+      - name: Pin Go version to mod file
+        uses: actions/setup-go@v5
+        with:
+          go-version-file: 'go.mod'
+          cache: true
+      - run: go version
+      - uses: actions/setup-node@v4
+        with:
+          node-version: 20
+          cache: 'yarn'
+      - name: Cache Node Modules
+        id: cache-node-modules
+        uses: actions/cache@v3
+        with:
+          path: |
+            node_modules
+            /home/runner/.cache/Cypress
+          key: ${{ runner.os }}-node-${{ hashFiles('package-lock.json') }}
+      - name: Install dependencies
+        if: steps.cache-node-modules.outputs.cache-hit != 'true'
+        run: yarn install --immutable
+      - name: Install Cypress dependencies
+        if: steps.cache-node-modules.outputs.cache-hit != 'true'
+        uses: cypress-io/github-action@v6
+        with:
+          runTests: false
+      - name: Cache Grafana Build and Dependencies
+        id: cache-grafana
+        uses: actions/cache@v3
+        with:
+          path: |
+            bin/
+            scripts/grafana-server/
+            tools/
+            public/
+            conf/
+            e2e/test-plugins/
+            devenv/
+          key: ${{ runner.os }}-grafana-${{ hashFiles('go.mod', 'package-lock.json', 'Makefile', 'pkg/storage/**/*.go', 'public/app/features/search/**/*.ts', 'public/app/features/search/**/*.tsx') }}
+      # only rebuild grafana if search files have changed ( or dependencies )
+      - name: Build Grafana (Runs Only If Not Cached)
+        if: steps.cache-grafana.outputs.cache-hit != 'true'
+        run: make build
+
+      - name: Get list of .ini files
+        id: get_files
+        run: |
+          INI_FILES=$(ls ${{ github.workspace }}/e2e/dashboards-search-suite/*.ini | jq -R -s -c 'split("\n")[:-1]')
+          echo "ini_files=$INI_FILES" >> $GITHUB_OUTPUT
+        shell: bash
+
+  run_tests:
+      needs: setup
+      runs-on: ubuntu-latest
+      continue-on-error: true
+      if: github.event.pull_request.draft == false
+      strategy:
+        matrix:
+          ini_file: ${{ fromJson(needs.setup.outputs.ini_files) }}
+
+      steps:
+        - name: Checkout repository
+          uses: actions/checkout@v4
+
+        - name: Restore Cached Node Modules
+          uses: actions/cache@v3
+          with:
+            path: |
+              node_modules
+              /home/runner/.cache/Cypress
+            key: foo
+
+        - name: Restore Cached Grafana Build and Dependencies
+          uses: actions/cache@v3
+          with:
+            path: |
+              bin/
+              scripts/grafana-server/
+              tools/
+              public/
+              conf/
+              e2e/test-plugins/
+              devenv/
+            key: ${{ runner.os }}-grafana-${{ hashFiles('go.mod', 'package-lock.json', 'Makefile', 'pkg/storage/**/*.go', 'public/app/features/search/**/*.ts', 'public/app/features/search/**/*.tsx') }}
+        - name: Prettify the name
+          run: echo "Running tests for $(basename "${{ matrix.ini_file }}")"
+        - name: Set the step name
+          id: set_file_name
+          run: |
+            FILE_NAME=$(basename "${{ matrix.ini_file }}" .ini)
+            echo "FILE_NAME=$FILE_NAME" >> $GITHUB_ENV
+        - name: Run tests for ${{ env.FILE_NAME }}
+          run: |
+            cp -rf ${{ matrix.ini_file }} ${{ github.workspace }}/scripts/grafana-server/custom.ini
+            yarn e2e:dashboards-search || echo "Test failed but marking as success since unified search is behind a feature flag and should not block PRs"
+        - name: Always succeed # This is a workaround to make the job pass even if the previous step fails
+          if: failure()
+          run: exit 0
diff --git a/e2e/dashboards-search-suite/dashboard-search.spec.ts b/e2e/dashboards-search-suite/dashboard-search.spec.ts
new file mode 100644
index 00000000000..e93f116dfff
--- /dev/null
+++ b/e2e/dashboards-search-suite/dashboard-search.spec.ts
@@ -0,0 +1,61 @@
+import { e2e } from '../utils';
+
+const rowGroup = '[role="rowgroup"]';
+const row = '[role="row"]';
+const searchInput = '[data-testid="input-wrapper"]';
+
+describe('Dashboard search', () => {
+  beforeEach(() => {
+    e2e.flows.login(Cypress.env('USERNAME'), Cypress.env('PASSWORD'));
+  });
+
+  it('Search - Dashboards list', () => {
+    e2e.pages.Dashboards.visit();
+
+    toggleSearchView();
+
+    assertResultsCount(24);
+  });
+
+  it('Search - Filter by search input', () => {
+    e2e.pages.Dashboards.visit();
+
+    toggleSearchView();
+
+    assertResultsCount(24);
+
+    // prefix match
+    cy.get(searchInput).type('Datasource tests - MySQL');
+    assertResultsCount(2);
+
+    cy.get(searchInput).type('{selectall}{backspace}'); // clear input
+
+    // exact match
+    cy.get(searchInput).type('Datasource tests - MySQL (unittest)');
+    assertResultsCount(1);
+
+    cy.get(searchInput).type('{selectall}{backspace}'); // clear input
+
+    // suffix match
+    cy.get(searchInput).type('- MySQL');
+    assertResultsCount(1);
+  });
+});
+
+const assertResultsCount = (length: number) => {
+  e2e.pages.SearchDashboards.table().should('exist');
+
+  const table = e2e.pages.SearchDashboards.table();
+  const group = table.find(rowGroup);
+  group.should('have.length', 1);
+  const rows = group.find(row);
+  rows.should('have.length', length);
+};
+
+const toggleSearchView = () => {
+  e2e.pages.Dashboards.toggleView().each((e, i) => {
+    if (i === 1) {
+      cy.wrap(e).click();
+    }
+  });
+};
diff --git a/e2e/dashboards-search-suite/mode0.ini b/e2e/dashboards-search-suite/mode0.ini
new file mode 100644
index 00000000000..752638f24f2
--- /dev/null
+++ b/e2e/dashboards-search-suite/mode0.ini
@@ -0,0 +1,19 @@
+[server]
+
+[feature_toggles]
+kubernetesFolders = true
+unifiedStorageSearch = true
+unifiedStorageSearchUI = true
+grafanaAPIServerWithExperimentalAPIs = true
+kubernetesDashboardsAPI = true
+kubernetesCliDashboards = true
+unifiedStorageSearchSprinkles = true
+kubernetesFoldersServiceV2 = true
+unifiedStorageSearchPermissionFiltering = true
+kubernetesClientDashboardsFolders = true
+
+[unified_storage.folders.folder.grafana.app]
+dualWriterMode = 0
+
+[unified_storage.dashboards.dashboard.grafana.app]
+dualWriterMode = 0
\ No newline at end of file
diff --git a/e2e/dashboards-search-suite/mode1.ini b/e2e/dashboards-search-suite/mode1.ini
new file mode 100644
index 00000000000..8f8f80e8e30
--- /dev/null
+++ b/e2e/dashboards-search-suite/mode1.ini
@@ -0,0 +1,19 @@
+[server]
+
+[feature_toggles]
+kubernetesFolders = true
+unifiedStorageSearch = true
+unifiedStorageSearchUI = true
+grafanaAPIServerWithExperimentalAPIs = true
+kubernetesDashboardsAPI = true
+kubernetesCliDashboards = true
+unifiedStorageSearchSprinkles = true
+kubernetesFoldersServiceV2 = true
+unifiedStorageSearchPermissionFiltering = true
+kubernetesClientDashboardsFolders = true
+
+[unified_storage.folders.folder.grafana.app]
+dualWriterMode = 1
+
+[unified_storage.dashboards.dashboard.grafana.app]
+dualWriterMode = 1
\ No newline at end of file
diff --git a/e2e/dashboards-search-suite/mode2-legacy-search-api.ini b/e2e/dashboards-search-suite/mode2-legacy-search-api.ini
new file mode 100644
index 00000000000..38590b40a67
--- /dev/null
+++ b/e2e/dashboards-search-suite/mode2-legacy-search-api.ini
@@ -0,0 +1,19 @@
+[server]
+
+[feature_toggles]
+kubernetesFolders = true
+unifiedStorageSearch = true
+unifiedStorageSearchUI = false
+grafanaAPIServerWithExperimentalAPIs = true
+kubernetesDashboardsAPI = true
+kubernetesCliDashboards = true
+unifiedStorageSearchSprinkles = true
+kubernetesFoldersServiceV2 = true
+unifiedStorageSearchPermissionFiltering = true
+kubernetesClientDashboardsFolders = true
+
+[unified_storage.folders.folder.grafana.app]
+dualWriterMode = 2
+
+[unified_storage.dashboards.dashboard.grafana.app]
+dualWriterMode = 2
\ No newline at end of file
diff --git a/e2e/dashboards-search-suite/mode2.ini b/e2e/dashboards-search-suite/mode2.ini
new file mode 100644
index 00000000000..c1d5890d6f4
--- /dev/null
+++ b/e2e/dashboards-search-suite/mode2.ini
@@ -0,0 +1,19 @@
+[server]
+
+[feature_toggles]
+kubernetesFolders = true
+unifiedStorageSearch = true
+unifiedStorageSearchUI = true
+grafanaAPIServerWithExperimentalAPIs = true
+kubernetesDashboardsAPI = true
+kubernetesCliDashboards = true
+unifiedStorageSearchSprinkles = true
+kubernetesFoldersServiceV2 = true
+unifiedStorageSearchPermissionFiltering = true
+kubernetesClientDashboardsFolders = true
+
+[unified_storage.folders.folder.grafana.app]
+dualWriterMode = 2
+
+[unified_storage.dashboards.dashboard.grafana.app]
+dualWriterMode = 2
\ No newline at end of file
diff --git a/e2e/dashboards-search-suite/mode3.ini b/e2e/dashboards-search-suite/mode3.ini
new file mode 100644
index 00000000000..e027f7e429f
--- /dev/null
+++ b/e2e/dashboards-search-suite/mode3.ini
@@ -0,0 +1,19 @@
+[server]
+
+[feature_toggles]
+kubernetesFolders = true
+unifiedStorageSearch = true
+unifiedStorageSearchUI = true
+grafanaAPIServerWithExperimentalAPIs = true
+kubernetesDashboardsAPI = true
+kubernetesCliDashboards = true
+unifiedStorageSearchSprinkles = true
+kubernetesFoldersServiceV2 = true
+unifiedStorageSearchPermissionFiltering = true
+kubernetesClientDashboardsFolders = true
+
+[unified_storage.folders.folder.grafana.app]
+dualWriterMode = 3
+
+[unified_storage.dashboards.dashboard.grafana.app]
+dualWriterMode = 3
\ No newline at end of file
diff --git a/e2e/dashboards-search-suite/mode4.ini b/e2e/dashboards-search-suite/mode4.ini
new file mode 100644
index 00000000000..4c00fd10c47
--- /dev/null
+++ b/e2e/dashboards-search-suite/mode4.ini
@@ -0,0 +1,19 @@
+[server]
+
+[feature_toggles]
+kubernetesFolders = true
+unifiedStorageSearch = true
+unifiedStorageSearchUI = true
+grafanaAPIServerWithExperimentalAPIs = true
+kubernetesDashboardsAPI = true
+kubernetesCliDashboards = true
+unifiedStorageSearchSprinkles = true
+kubernetesFoldersServiceV2 = true
+unifiedStorageSearchPermissionFiltering = true
+kubernetesClientDashboardsFolders = true
+
+[unified_storage.folders.folder.grafana.app]
+dualWriterMode = 4
+
+[unified_storage.dashboards.dashboard.grafana.app]
+dualWriterMode = 4
\ No newline at end of file
diff --git a/e2e/dashboards-search-suite/mode5.ini b/e2e/dashboards-search-suite/mode5.ini
new file mode 100644
index 00000000000..277d4cdf1c1
--- /dev/null
+++ b/e2e/dashboards-search-suite/mode5.ini
@@ -0,0 +1,19 @@
+[server]
+
+[feature_toggles]
+kubernetesFolders = true
+unifiedStorageSearch = true
+unifiedStorageSearchUI = true
+grafanaAPIServerWithExperimentalAPIs = true
+kubernetesDashboardsAPI = true
+kubernetesCliDashboards = true
+unifiedStorageSearchSprinkles = true
+kubernetesFoldersServiceV2 = true
+unifiedStorageSearchPermissionFiltering = true
+kubernetesClientDashboardsFolders = true
+
+[unified_storage.folders.folder.grafana.app]
+dualWriterMode = 5
+
+[unified_storage.dashboards.dashboard.grafana.app]
+dualWriterMode = 5
\ No newline at end of file
diff --git a/e2e/run-suite b/e2e/run-suite
index ef649a6c6c4..28ed2f6bd8d 100755
--- a/e2e/run-suite
+++ b/e2e/run-suite
@@ -29,6 +29,7 @@ testFilesForSingleSuite="*.spec.ts"
 rootForEnterpriseSuite="./e2e/extensions-suite"
 rootForOldArch="./e2e/old-arch"
 rootForKubernetesDashboards="./e2e/dashboards-suite"
+rootForSearchDashboards="./e2e/dashboards-search-suite"
 
 declare -A cypressConfig=(
   [screenshotsFolder]=./e2e/"${args[0]}"/screenshots
@@ -130,6 +131,24 @@ case "$1" in
                 ;;
           esac
       ;;
+    "dashboards-search")
+      env[kubernetesDashboards]=true
+      cypressConfig[specPattern]=$rootForSearchDashboards/$testFilesForSingleSuite
+      cypressConfig[video]=false
+          case "$2" in
+            "debug")
+                echo -e "Debug mode"
+                env[SLOWMO]=1
+                PARAMS="--no-exit"
+                enterpriseSuite=$(basename "${args[2]}")
+                ;;
+            "dev")
+                echo "Dev mode"
+                CMD="cypress open"
+                enterpriseSuite=$(basename "${args[2]}")
+                ;;
+          esac
+      ;;
    "enterprise-smtp")
       env[SMTP_PLUGIN_ENABLED]=true
       cypressConfig[specPattern]=./e2e/extensions/enterprise/smtp-suite/$testFilesForSingleSuite
diff --git a/package.json b/package.json
index 21e0b67bc64..e38de177c7f 100644
--- a/package.json
+++ b/package.json
@@ -13,6 +13,7 @@
     "e2e": "./e2e/start-and-run-suite",
     "e2e:old-arch": "./e2e/start-and-run-suite old-arch",
     "e2e:schema-v2": "./e2e/start-and-run-suite dashboards-schema-v2",
+    "e2e:dashboards-search": "./e2e/start-and-run-suite dashboards-search",
     "e2e:debug": "./e2e/start-and-run-suite debug",
     "e2e:dev": "./e2e/start-and-run-suite dev",
     "e2e:benchmark:live": "./e2e/start-and-run-suite benchmark live",
diff --git a/packages/grafana-e2e-selectors/src/selectors/pages.ts b/packages/grafana-e2e-selectors/src/selectors/pages.ts
index 2e63f0f21c4..bd45587a7bc 100644
--- a/packages/grafana-e2e-selectors/src/selectors/pages.ts
+++ b/packages/grafana-e2e-selectors/src/selectors/pages.ts
@@ -569,6 +569,9 @@ export const versionedPages = {
     dashboards: {
       '10.2.0': (title: string) => `Dashboard search item ${title}`,
     },
+    toggleView: {
+      [MIN_GRAFANA_VERSION]: 'data-testid radio-button',
+    },
   },
   SaveDashboardAsModal: {
     newName: {
@@ -945,6 +948,11 @@ export const versionedPages = {
       },
     },
   },
+  SearchDashboards: {
+    table: {
+      '10.2.0': 'Search results table',
+    },
+  },
   Search: {
     url: {
       '9.3.0': '/?search=openn',