diff --git a/public/app/features/dashboard/api/v1.test.ts b/public/app/features/dashboard/api/v1.test.ts
index 675010235ef..20c6699d13b 100644
--- a/public/app/features/dashboard/api/v1.test.ts
+++ b/public/app/features/dashboard/api/v1.test.ts
@@ -144,6 +144,7 @@ describe('v1 dashboard API', () => {
 
     const api = new K8sDashboardAPI();
     const result = await api.getDashboardDTO('test');
+    expect(result.meta.slug).toBe('test');
     expect(result.meta.isFolder).toBe(false);
     expect(result.meta.folderId).toBe(1);
     expect(result.meta.folderTitle).toBe('New Folder');
@@ -204,6 +205,7 @@ describe('v1 dashboard API', () => {
         });
 
         expect(result.uid).toBe('adh59cn');
+        expect(result.slug).toBe('new-dashboard-saved');
         expect(result.version).toBe(1);
         expect(result.url).toBe('/d/adh59cn/new-dashboard-saved');
       });
@@ -229,6 +231,7 @@ describe('v1 dashboard API', () => {
           folderUid: 'test',
         });
 
+        expect(result.slug).toBe('new-dashboard-saved');
         expect(result.uid).toBe('adh59cn');
         expect(result.version).toBe(1);
         expect(result.url).toBe('/grafana/d/adh59cn/new-dashboard-saved');
@@ -248,6 +251,7 @@ describe('v1 dashboard API', () => {
         });
 
         expect(result.uid).toBe('adh59cn');
+        expect(result.slug).toBe('new-dashboard-saved');
         expect(result.version).toBe(1);
         expect(result.url).toBe('/d/adh59cn/new-dashboard-saved');
       });
@@ -274,6 +278,7 @@ describe('v1 dashboard API', () => {
         });
 
         expect(result.uid).toBe('adh59cn');
+        expect(result.slug).toBe('new-dashboard-saved');
         expect(result.version).toBe(1);
         expect(result.url).toBe('/grafana/d/adh59cn/new-dashboard-saved');
       });
diff --git a/public/app/features/dashboard/api/v1.ts b/public/app/features/dashboard/api/v1.ts
index 7b6423adc3e..d58fa1d78a7 100644
--- a/public/app/features/dashboard/api/v1.ts
+++ b/public/app/features/dashboard/api/v1.ts
@@ -86,11 +86,13 @@ export class K8sDashboardAPI implements DashboardAPI<DashboardDTO, Dashboard> {
   }
 
   asSaveDashboardResponseDTO(v: Resource<DashboardDataDTO>): SaveDashboardResponseDTO {
+    const slug = kbn.slugifyForUrl(v.spec.title.trim());
+
     const url = locationUtil.assureBaseUrl(
       getDashboardUrl({
         uid: v.metadata.name,
         currentQueryParams: '',
-        slug: kbn.slugifyForUrl(v.spec.title.trim()),
+        slug,
       })
     );
 
@@ -100,7 +102,7 @@ export class K8sDashboardAPI implements DashboardAPI<DashboardDTO, Dashboard> {
       id: v.spec.id ?? 0,
       status: 'success',
       url,
-      slug: '',
+      slug,
     };
   }
 
@@ -124,6 +126,7 @@ export class K8sDashboardAPI implements DashboardAPI<DashboardDTO, Dashboard> {
       const result: DashboardDTO = {
         meta: {
           ...dash.access,
+          slug: kbn.slugifyForUrl(dash.spec.title.trim()),
           isNew: false,
           isFolder: false,
           uid: dash.metadata.name,
diff --git a/public/app/features/dashboard/api/v2.test.ts b/public/app/features/dashboard/api/v2.test.ts
index cb86f4d7467..b06387f6770 100644
--- a/public/app/features/dashboard/api/v2.test.ts
+++ b/public/app/features/dashboard/api/v2.test.ts
@@ -178,7 +178,7 @@ describe('v2 dashboard API', () => {
         id: 123,
         uid: 'test-dash',
         url: '/d/test-dash/testdashboard',
-        slug: '',
+        slug: 'testdashboard',
         status: 'success',
         version: 2,
       });
@@ -198,6 +198,7 @@ describe('v2 dashboard API', () => {
           name: 'existing-dash',
         },
       });
+      expect(result.slug).toBe('chaingtitledashboard');
       expect(result.version).toBe(2);
     });
 
diff --git a/public/app/features/dashboard/api/v2.ts b/public/app/features/dashboard/api/v2.ts
index 3cb7dc51468..3e0768992dd 100644
--- a/public/app/features/dashboard/api/v2.ts
+++ b/public/app/features/dashboard/api/v2.ts
@@ -73,6 +73,12 @@ export class K8sDashboardV2API
         dashboard.metadata.annotations[AnnoKeyFolder] = '';
       }
 
+      // Ensure a consistent dashboard slug
+      if (!dashboard.access?.slug) {
+        dashboard.access = dashboard.access ?? {};
+        dashboard.access.slug = kbn.slugifyForUrl(dashboard.spec.title.trim());
+      }
+
       return dashboard;
     } catch (e) {
       const status = getStatusFromError(e);
@@ -145,11 +151,13 @@ export class K8sDashboardV2API
   }
 
   asSaveDashboardResponseDTO(v: Resource<DashboardV2Spec>): SaveDashboardResponseDTO {
+    const slug = kbn.slugifyForUrl(v.spec.title.trim());
+
     const url = locationUtil.assureBaseUrl(
       getDashboardUrl({
         uid: v.metadata.name,
         currentQueryParams: '',
-        slug: kbn.slugifyForUrl(v.spec.title.trim()),
+        slug,
       })
     );
 
@@ -164,7 +172,7 @@ export class K8sDashboardV2API
       id: dashId,
       status: 'success',
       url,
-      slug: '',
+      slug,
     };
   }