diff --git a/dotcom-rendering/src/components/PuzzlesDirectory.test.tsx b/dotcom-rendering/src/components/PuzzlesDirectory.test.tsx
index 9cee38c9234..46f3d16fdb3 100644
--- a/dotcom-rendering/src/components/PuzzlesDirectory.test.tsx
+++ b/dotcom-rendering/src/components/PuzzlesDirectory.test.tsx
@@ -8,11 +8,6 @@ import type {
 } from '../types/puzzlesPage';
 import { getPuzzleUrl, PuzzlesDirectory } from './PuzzlesDirectory';
 
-jest.mock('./AdSlot.web', () => ({
-	AdSlot: ({ index }: { index: number }) => (
-		<div data-testid={`ad-${index}`} />
-	),
-}));
 jest.mock('./Island', () => ({
 	Island: ({ children }: { children: ReactNode }) => children,
 }));
@@ -38,6 +33,36 @@ const section = (
 });
 
 describe('PuzzlesDirectory', () => {
+	it('renders unique desktop and mobile IDs for multiple blueprint slots', () => {
+		const layout: PuzzlesLayoutType = {
+			containers: ['inline1', 'inline2'].map((adSlot) =>
+				section({
+					id: adSlot,
+					title: '',
+					variant: 'ad',
+					adSlot,
+					content: { items: [], nestedContainers: [] },
+				}),
+			),
+		};
+		const { rerender } = render(
+			<PuzzlesDirectory layout={layout} renderAds={true} />,
+		);
+		const ids = Array.from(
+			document.querySelectorAll('.js-ad-slot'),
+			({ id }) => id,
+		);
+		expect(ids).toEqual([
+			'dfp-ad--fronts-banner-1',
+			'dfp-ad--inline1--mobile',
+			'dfp-ad--fronts-banner-2',
+			'dfp-ad--inline2--mobile',
+		]);
+		expect(new Set(ids).size).toBe(ids.length);
+		rerender(<PuzzlesDirectory layout={layout} renderAds={false} />);
+		expect(document.querySelector('.js-ad-slot')).not.toBeInTheDocument();
+	});
+
 	it('does not render a disabled featured container', () => {
 		render(
 			<PuzzlesDirectory
@@ -176,9 +201,14 @@ describe('PuzzlesDirectory', () => {
 			screen.queryByRole('heading', { name: 'Empty' }),
 		).not.toBeInTheDocument();
 		expect(document.querySelector('img')).not.toBeInTheDocument();
-		expect(screen.queryByTestId('ad-2')).not.toBeInTheDocument();
+		expect(document.querySelector('.js-ad-slot')).not.toBeInTheDocument();
 		rerender(<PuzzlesDirectory layout={layout} renderAds={true} />);
-		expect(screen.getByTestId('ad-2')).toBeInTheDocument();
+		expect(
+			document.getElementById('dfp-ad--fronts-banner-2'),
+		).toHaveAttribute('data-name', 'fronts-banner-2');
+		expect(
+			document.getElementById('dfp-ad--inline2--mobile'),
+		).toHaveAttribute('data-name', 'inline2');
 	});
 
 	it('renders the archive dropdown and closes it with Escape or an outside click', async () => {
diff --git a/dotcom-rendering/src/components/PuzzlesDirectory.tsx b/dotcom-rendering/src/components/PuzzlesDirectory.tsx
index a4736e7a9e8..acd5d476df7 100644
--- a/dotcom-rendering/src/components/PuzzlesDirectory.tsx
+++ b/dotcom-rendering/src/components/PuzzlesDirectory.tsx
@@ -416,6 +416,7 @@ export const PuzzlesDirectory = ({ layout, renderAds }: Props) => (
 							index={index}
 							position="fronts-banner"
 						/>
+						<AdSlot position="mobile-front" index={index} />
 					</div>
 				);
 			}
diff --git a/dotcom-rendering/src/layouts/PuzzlesLayout.test.tsx b/dotcom-rendering/src/layouts/PuzzlesLayout.test.tsx
index aecafa32296..ef796d8400c 100644
--- a/dotcom-rendering/src/layouts/PuzzlesLayout.test.tsx
+++ b/dotcom-rendering/src/layouts/PuzzlesLayout.test.tsx
@@ -6,9 +6,6 @@ import { PuzzlesLayout } from './PuzzlesLayout';
 jest.mock('../components/Masthead/Masthead', () => ({
 	Masthead: () => <header data-testid="masthead" />,
 }));
-jest.mock('../components/HeaderAdSlot', () => ({
-	HeaderAdSlot: () => <div data-testid="header-ad" />,
-}));
 jest.mock('../components/Footer', () => ({
 	Footer: () => <div data-testid="footer" />,
 }));
@@ -51,12 +48,17 @@ describe('PuzzlesLayout', () => {
 		const { rerender } = render(
 			<PuzzlesLayout NAV={nav} puzzlesPage={page(true) as never} />,
 		);
-		expect(screen.queryByTestId('header-ad')).not.toBeInTheDocument();
+		expect(document.querySelector('.js-ad-slot')).not.toBeInTheDocument();
 		expect(screen.getByTestId('masthead')).toBeInTheDocument();
 		expect(screen.getByTestId('footer')).toBeInTheDocument();
 		rerender(
 			<PuzzlesLayout NAV={nav} puzzlesPage={page(false) as never} />,
 		);
-		expect(screen.getByTestId('header-ad')).toBeInTheDocument();
+		expect(
+			document.getElementById('dfp-ad--top-above-nav'),
+		).toBeInTheDocument();
+		expect(
+			document.getElementById('dfp-ad--mobile-above-nav'),
+		).not.toBeInTheDocument();
 	});
 });
diff --git a/dotcom-rendering/src/model/validate.puzzlesPage.test.ts b/dotcom-rendering/src/model/validate.puzzlesPage.test.ts
index d28f902092b..141f482d64b 100644
--- a/dotcom-rendering/src/model/validate.puzzlesPage.test.ts
+++ b/dotcom-rendering/src/model/validate.puzzlesPage.test.ts
@@ -38,6 +38,68 @@ const validPage = () => ({
 });
 
 describe('validateAsPuzzlesPageType', () => {
+	it.each(['inline1', 'mostpop'])(
+		'rejects repeated %s slot names',
+		(adSlot) => {
+			const page = validPage();
+			const container = {
+				id: 'first-ad',
+				title: '',
+				variant: adSlot === 'mostpop' ? 'supporting' : 'ad',
+				adSlot,
+				content: { items: [], nestedContainers: [] },
+				...(adSlot === 'mostpop'
+					? {
+							supporting: {
+								usefulLinksTitle: 'Useful links',
+								usefulLinks: [],
+								popularTitle: 'Most popular puzzles',
+								popularGroups: [],
+							},
+						}
+					: {}),
+			};
+			page.layout.containers.push(container as never);
+			expect(validateAsPuzzlesPageType(page)).toBeDefined();
+			page.layout.containers.push({
+				...container,
+				id: 'second-ad',
+			} as never);
+			expect(() => validateAsPuzzlesPageType(page)).toThrow(
+				'Unable to validate request body for puzzles page',
+			);
+		},
+	);
+
+	it.each(['inline0', 'inline-1', 'hub-inline', 'inline1junk', undefined])(
+		'rejects an unsupported ad slot: %s',
+		(adSlot) => {
+			const page = validPage();
+			page.layout.containers.push({
+				id: 'invalid-ad',
+				title: '',
+				variant: 'ad',
+				adSlot,
+				content: { items: [], nestedContainers: [] },
+			} as never);
+			expect(() => validateAsPuzzlesPageType(page)).toThrow();
+		},
+	);
+
+	it('accepts distinct inline slot names', () => {
+		const page = validPage();
+		for (const adSlot of ['inline1', 'inline2']) {
+			page.layout.containers.push({
+				id: adSlot,
+				title: '',
+				variant: 'ad',
+				adSlot,
+				content: { items: [], nestedContainers: [] },
+			} as never);
+		}
+		expect(validateAsPuzzlesPageType(page)).toBeDefined();
+	});
+
 	it('accepts a valid recursive blueprint contract', () => {
 		expect(
 			validateAsPuzzlesPageType(validPage()).layout.containers[0]?.id,
diff --git a/dotcom-rendering/src/model/validate.ts b/dotcom-rendering/src/model/validate.ts
index f958421ea0c..60480796519 100644
--- a/dotcom-rendering/src/model/validate.ts
+++ b/dotcom-rendering/src/model/validate.ts
@@ -354,6 +354,9 @@ export const validateAsPuzzlesPageType = (data: unknown): FEPuzzlesPageType => {
 	const unique = (values: string[]) => new Set(values).size === values.length;
 	const containerIds = containers.map(({ id }) => id);
 	const itemIds = items.map(({ id }) => id);
+	const adSlots = containers.flatMap(({ adSlot }) =>
+		adSlot === undefined ? [] : [adSlot],
+	);
 	const popularReferencesValid = containers.every((container) =>
 		(container.supporting?.popularGroups ?? []).every((group) =>
 			group.itemIds.every((id) => itemIds.includes(id)),
@@ -366,6 +369,7 @@ export const validateAsPuzzlesPageType = (data: unknown): FEPuzzlesPageType => {
 	if (
 		!unique(containerIds) ||
 		!unique(itemIds) ||
+		!unique(adSlots) ||
 		!popularReferencesValid ||
 		!topLevelOnlyContainersValid
 	) {