diff --git a/.changeset/quiet-404-rewrite-cache.md b/.changeset/quiet-404-rewrite-cache.md
new file mode 100644
index 0000000000..a9afd74808
--- /dev/null
+++ b/.changeset/quiet-404-rewrite-cache.md
@@ -0,0 +1,5 @@
+---
+"emdash": patch
+---
+
+Fixes duplicate layout queries when anonymous public pages call `Astro.rewrite()`, such as rewriting an unknown slug to `/404`. The rewritten page reuses the original request's cached reads and prefetched layout data. Previews, edit mode, signed-in requests, and rewrites that change locale continue to use fresh request contexts.
diff --git a/packages/core/src/astro/middleware.ts b/packages/core/src/astro/middleware.ts
index 01f2b6ba61..7a87fb69d2 100644
--- a/packages/core/src/astro/middleware.ts
+++ b/packages/core/src/astro/middleware.ts
@@ -758,6 +758,44 @@ function keepUnsharedResponsesOutOfRouteCache(context: APIContext, response: Res
 	}
 }
 
+const ANONYMOUS_RENDER = Symbol.for("emdash:anonymous-render");
+
+type RenderLocals = App.Locals & {
+	[ANONYMOUS_RENDER]?: {
+		method: string;
+		locale: string | undefined;
+		db: unknown;
+		metrics: RequestMetrics | undefined;
+	};
+};
+
+function canReuseAnonymousRender(context: APIContext): boolean {
+	const original = (context.locals as RenderLocals)[ANONYMOUS_RENDER];
+	const parent = getRequestContext();
+	if (!original || !parent) return false;
+	if (context.request.method !== original.method) return false;
+	if (context.currentLocale !== original.locale) return false;
+	if (context.locals.__playgroundDb || context.locals.user || parent.editMode || parent.preview)
+		return false;
+	if (parent.db !== original.db || parent.metrics !== original.metrics) return false;
+	if (context.request.headers.has("authorization")) return false;
+	if (context.cookies.get(virtualConfig?.sessionCookieName ?? "astro-session")) return false;
+	if (context.cookies.get("emdash-edit-mode")?.value === "true") return false;
+	if (context.url.searchParams.has("_preview")) return false;
+	if (context.url.pathname.startsWith("/_emdash") || isImageEndpointRequest(context)) return false;
+	const base = import.meta.env.BASE_URL.replace(TRAILING_SLASH_RE, "");
+	const path =
+		base && context.url.pathname.startsWith(`${base}/`)
+			? context.url.pathname.slice(base.length)
+			: context.url.pathname;
+	if (PUBLIC_RUNTIME_ROUTES.has(path) || isCollectionSitemapPath(path)) return false;
+	// A newly cacheable target must not reuse data loaded from an unverified object-cache snapshot.
+	if (virtualConfig?.objectCacheEnabled && context.cache?.enabled && !parent.routeCacheFill) {
+		return false;
+	}
+	return true;
+}
+
 export const onRequest = defineMiddleware(async (context, next) => {
 	const { request, locals, cookies } = context;
 	const url = context.url;
@@ -776,6 +814,10 @@ export const onRequest = defineMiddleware(async (context, next) => {
 		}
 	}
 
+	// Astro re-enters middleware with the same locals while the original render is
+	// still active. Its outer scope owns prefetch, metrics, and connection cleanup.
+	if (canReuseAnonymousRender(context)) return next();
+
 	const queryRecorder = isInstrumentationEnabled()
 		? createRecorder(url.pathname, request.method, request.headers.get("x-perf-phase") ?? "default")
 		: undefined;
@@ -980,7 +1022,22 @@ export const onRequest = defineMiddleware(async (context, next) => {
 				});
 				const runAnon = async () => {
 					const t0 = performance.now();
-					const response = await next();
+					const renderLocals = locals as RenderLocals;
+					const previous = renderLocals[ANONYMOUS_RENDER];
+					const scope = getRequestContext();
+					renderLocals[ANONYMOUS_RENDER] = {
+						method: request.method,
+						locale: context.currentLocale,
+						db: scope?.db,
+						metrics: scope?.metrics,
+					};
+					let response: Response;
+					try {
+						response = await next();
+					} finally {
+						if (previous) renderLocals[ANONYMOUS_RENDER] = previous;
+						else delete renderLocals[ANONYMOUS_RENDER];
+					}
 					timings.push({ name: "render", dur: performance.now() - t0, desc: "Page render" });
 					timings.push({ name: "mw", dur: performance.now() - mwStart, desc: "Total middleware" });
 					pushMetricsTimings(timings, metrics);
diff --git a/packages/core/src/astro/middleware/redirect.ts b/packages/core/src/astro/middleware/redirect.ts
index 8e5e0cb957..6e4bc95a56 100644
--- a/packages/core/src/astro/middleware/redirect.ts
+++ b/packages/core/src/astro/middleware/redirect.ts
@@ -301,8 +301,14 @@ export const onRequest = defineMiddleware(async (context, next) => {
 	if (!routeCache?.enabled) return run();
 	const parent = getRequestContext();
 	if (parent) {
+		const previousSettings = parent.siteSettings;
+		requestSettings.live = parent.routeCacheFill === true;
 		parent.siteSettings = requestSettings;
-		return run();
+		try {
+			return await run();
+		} finally {
+			if (previousSettings) parent.siteSettings = previousSettings;
+		}
 	}
 	return runWithContext({ editMode: false, siteSettings: requestSettings }, run);
 });
diff --git a/packages/core/src/astro/middleware/request-context.ts b/packages/core/src/astro/middleware/request-context.ts
index 735e20807c..3572023b56 100644
--- a/packages/core/src/astro/middleware/request-context.ts
+++ b/packages/core/src/astro/middleware/request-context.ts
@@ -302,6 +302,7 @@ export const onRequest = defineMiddleware(async (context, next) => {
 		if (virtualConfig?.objectCacheEnabled && context.cache?.enabled) {
 			const parent = getRequestContext();
 			if (parent?.siteSettings) parent.siteSettings.live = true;
+			if (parent?.routeCacheFill) return render();
 			return runWithContext({ ...parent, editMode: false, routeCacheFill: true }, render);
 		}
 		return render();
diff --git a/packages/core/tests/unit/astro/middleware-layout-prefetch.test.ts b/packages/core/tests/unit/astro/middleware-layout-prefetch.test.ts
index 23cdba5101..c04ff9c105 100644
--- a/packages/core/tests/unit/astro/middleware-layout-prefetch.test.ts
+++ b/packages/core/tests/unit/astro/middleware-layout-prefetch.test.ts
@@ -1,3 +1,5 @@
+import { experimental_AstroContainer as AstroContainer } from "astro/container";
+import { createAstro, createComponent, render } from "astro/runtime/server/index.js";
 import {
 	type DialectAdapter,
 	DummyDriver,
@@ -7,7 +9,10 @@ import {
 	SqliteIntrospector,
 	SqliteQueryCompiler,
 } from "kysely";
-import { beforeEach, describe, it, expect, vi } from "vitest";
+import { afterAll, beforeAll, beforeEach, describe, it, expect, vi } from "vitest";
+
+import { requestCached } from "../../../src/request-cache.js";
+import { setupTestDatabase, teardownTestDatabase } from "../../utils/test-db.js";
 
 vi.mock("astro:middleware", () => ({
 	defineMiddleware: (handler: unknown) => handler,
@@ -21,6 +26,7 @@ const { MOCK_RUNTIME, createRequestScopedDb, prefetchLayoutData } = vi.hoisted((
 		MOCK_RUNTIME: {
 			storage: { getPublicUrl: vi.fn((key: string) => `https://media.example.com/${key}`) },
 			db: {},
+			rooms: null,
 			hooks: {},
 			email: null,
 			configuredPlugins: [],
@@ -47,9 +53,13 @@ vi.mock(
 	() => ({ default: { database: { config: { binding: "DB" } }, auth: { mode: "none" } } }),
 	{ virtual: true },
 );
-vi.mock("virtual:emdash/dialect", () => ({ createDialect: vi.fn(), createRequestScopedDb }), {
-	virtual: true,
-});
+vi.mock(
+	"virtual:emdash/dialect",
+	() => ({ createDialect: vi.fn(), createCoalescingDialect: null, createRequestScopedDb }),
+	{
+		virtual: true,
+	},
+);
 vi.mock("virtual:emdash/media-providers", () => ({ mediaProviders: [] }), { virtual: true });
 vi.mock("virtual:emdash/plugins", () => ({ plugins: [] }), { virtual: true });
 vi.mock(
@@ -64,7 +74,17 @@ vi.mock("virtual:emdash/scheduler", () => ({ createScheduler: null }), { virtual
 
 vi.mock("../../../src/emdash-runtime.js", () => ({
 	DB_INIT_DEADLINE_MS: 30_000,
-	EmDashRuntime: { create: async () => MOCK_RUNTIME },
+	EmDashRuntime: {
+		create: async () =>
+			new Proxy(MOCK_RUNTIME, {
+				get: (runtime, key) =>
+					key === "then"
+						? undefined
+						: key in runtime
+							? Reflect.get(runtime, key)
+							: async () => ({ success: true }),
+			}),
+	},
 }));
 
 vi.mock("../../../src/loader.js", () => ({
@@ -88,14 +108,19 @@ function kyselyWith(adapter: DialectAdapter) {
 	});
 }
 
-function htmlNavigation() {
+function htmlNavigation(
+	path = "/posts/hello",
+	locals: Record<string, unknown> = {},
+	properties: Record<string, unknown> = {},
+) {
 	return {
-		request: new Request("https://example.com/posts/hello", {
+		request: new Request(`https://example.com${path}`, {
 			headers: { accept: "text/html,application/xhtml+xml" },
 		}),
-		url: new URL("https://example.com/posts/hello"),
+		url: new URL(`https://example.com${path}`),
 		cookies: { get: vi.fn(() => undefined), set: vi.fn() },
-		locals: {} as Record<string, unknown>,
+		locals,
+		...properties,
 		redirect: vi.fn(),
 		isPrerendered: false,
 		session: { get: vi.fn(async () => null) },
@@ -111,8 +136,30 @@ async function navigate() {
 }
 
 describe("layout prefetch on anonymous HTML navigations", () => {
+	let realDb: Awaited<ReturnType<typeof setupTestDatabase>>;
+	let queryCount: ReturnType<typeof vi.spyOn>;
+
+	beforeAll(async () => {
+		realDb = await setupTestDatabase();
+		Object.defineProperty(realDb.getExecutor().adapter, "supportsMultipleConnections", {
+			value: true,
+		});
+		queryCount = vi.spyOn(realDb.getExecutor(), "executeQuery");
+	});
+
+	afterAll(async () => {
+		queryCount.mockRestore();
+		await teardownTestDatabase(realDb);
+	});
+
 	beforeEach(() => {
 		vi.clearAllMocks();
+		queryCount.mockClear();
+		prefetchLayoutData.mockImplementation(() =>
+			requestCached("rewrite-layout", async () =>
+				realDb.selectFrom("_emdash_migrations").selectAll().limit(1).execute(),
+			).then(() => undefined),
+		);
 	});
 
 	const adapterWithoutFlag: DialectAdapter = {
@@ -139,4 +186,148 @@ describe("layout prefetch on anonymous HTML navigations", () => {
 		expect(createRequestScopedDb).toHaveBeenCalled();
 		expect(prefetchLayoutData).not.toHaveBeenCalled();
 	});
+
+	async function rewrite(
+		options: {
+			targetLocals?: Record<string, unknown>;
+			targetPath?: string;
+			targetProperties?: Record<string, unknown>;
+		} = {},
+	) {
+		const scope = { db: realDb, commit: vi.fn(), close: vi.fn() };
+		createRequestScopedDb.mockReturnValue(scope);
+		const original = htmlNavigation("/missing-page");
+		const response = await onRequest(original, async () => {
+			await requestCached("rewrite-layout", async () =>
+				realDb.selectFrom("_emdash_migrations").selectAll().limit(1).execute(),
+			);
+			const target = htmlNavigation(
+				options.targetPath ?? "/404",
+				options.targetLocals ?? original.locals,
+				options.targetProperties,
+			);
+			return onRequest(target, async () => {
+				await requestCached("rewrite-layout", async () =>
+					realDb.selectFrom("_emdash_migrations").selectAll().limit(1).execute(),
+				);
+				return new Response("ok");
+			});
+		});
+		await response.text();
+		await new Promise((resolve) => setTimeout(resolve, 10));
+		return scope;
+	}
+
+	it("does not repeat layout reads through Astro's real rewrite pipeline", async () => {
+		const scope = { db: realDb, commit: vi.fn(), close: vi.fn() };
+		createRequestScopedDb.mockReturnValue(scope);
+		const read = () =>
+			requestCached("rewrite-layout", async () =>
+				realDb.selectFrom("_emdash_migrations").selectAll().limit(1).execute(),
+			);
+		const notFound = createComponent(async (result, props, slots) => {
+			const Astro = result.createAstro(createAstro(), props, slots);
+			Astro.response.status = 404;
+			await read();
+			return render`<html><body>Not found</body></html>`;
+		});
+		const missing = createComponent(async (result, props, slots) => {
+			const Astro = result.createAstro(createAstro(), props, slots);
+			await read();
+			return Astro.rewrite("/404");
+		});
+		const container = await AstroContainer.create({
+			manifest: {
+				middleware: async () => ({ onRequest }),
+			} as NonNullable<Parameters<typeof AstroContainer.create>[0]>["manifest"],
+		});
+		container.insertPageRoute("/404", notFound);
+		const direct = await container.renderToResponse(notFound, {
+			request: new Request("https://example.com/404", { headers: { accept: "text/html" } }),
+		});
+		expect(direct.status).toBe(404);
+		await direct.text();
+		await new Promise((resolve) => setTimeout(resolve, 10));
+		const directQueries = queryCount.mock.calls.length;
+		vi.clearAllMocks();
+		const rewritten = await container.renderToResponse(missing, {
+			request: new Request("https://example.com/missing-page", {
+				headers: { accept: "text/html" },
+			}),
+		});
+		expect(rewritten.status).toBe(404);
+		expect(await rewritten.text()).toContain("Not found");
+		await new Promise((resolve) => setTimeout(resolve, 10));
+		expect(directQueries).toBe(1);
+		expect(queryCount).toHaveBeenCalledTimes(directQueries);
+		expect(prefetchLayoutData).toHaveBeenCalledOnce();
+		expect(createRequestScopedDb).toHaveBeenCalledOnce();
+		expect(scope.commit).toHaveBeenCalledOnce();
+		expect(scope.close).toHaveBeenCalledOnce();
+	});
+
+	it("reuses the prefetched layout read for an anonymous rewrite", async () => {
+		const scope = await rewrite();
+
+		expect(queryCount).toHaveBeenCalledOnce();
+		expect(prefetchLayoutData).toHaveBeenCalledOnce();
+		expect(createRequestScopedDb).toHaveBeenCalledOnce();
+		expect(scope.commit).toHaveBeenCalledOnce();
+		expect(scope.close).toHaveBeenCalledOnce();
+	});
+
+	it("does not reuse the cache across independent requests", async () => {
+		await rewrite();
+		await rewrite();
+
+		expect(queryCount).toHaveBeenCalledTimes(2);
+		expect(prefetchLayoutData).toHaveBeenCalledTimes(2);
+		expect(createRequestScopedDb).toHaveBeenCalledTimes(2);
+	});
+
+	it("does not reuse the cache when the rewrite has different locals", async () => {
+		await rewrite({ targetLocals: {} });
+
+		expect(queryCount).toHaveBeenCalledTimes(2);
+		expect(createRequestScopedDb).toHaveBeenCalledTimes(2);
+	});
+
+	it("does not reuse the cache for a different locale target", async () => {
+		await rewrite({ targetProperties: { currentLocale: "fr" } });
+
+		expect(queryCount).toHaveBeenCalledTimes(2);
+	});
+
+	it.each(["/_emdash/api/content", "/sitemap.xml"])(
+		"initializes runtime handlers for a rewrite to %s",
+		async (targetPath) => {
+			await rewrite({ targetPath });
+			expect(queryCount).toHaveBeenCalledTimes(2);
+			expect(createRequestScopedDb).toHaveBeenCalledTimes(2);
+		},
+	);
+
+	it("does not reuse the cache for a preview target", async () => {
+		await rewrite({ targetPath: "/404?_preview=1" });
+
+		expect(queryCount).toHaveBeenCalledTimes(2);
+	});
+
+	it("closes the scoped database when the rewritten render fails", async () => {
+		const scope = { db: realDb, commit: vi.fn(), close: vi.fn() };
+		createRequestScopedDb.mockReturnValue(scope);
+		const original = htmlNavigation("/missing-page");
+		await expect(
+			onRequest(original, async () =>
+				onRequest(htmlNavigation("/404", original.locals, {}), async () => {
+					throw new Error("render failed");
+				}),
+			),
+		).rejects.toThrow("render failed");
+		await new Promise((resolve) => setTimeout(resolve, 10));
+
+		expect(createRequestScopedDb).toHaveBeenCalledOnce();
+		expect(scope.commit).toHaveBeenCalledOnce();
+		expect(scope.close).toHaveBeenCalledOnce();
+	});
 });
diff --git a/packages/core/tests/unit/astro/middleware-redirect.test.ts b/packages/core/tests/unit/astro/middleware-redirect.test.ts
index e8a3aba711..43c2823d2c 100644
--- a/packages/core/tests/unit/astro/middleware-redirect.test.ts
+++ b/packages/core/tests/unit/astro/middleware-redirect.test.ts
@@ -25,6 +25,8 @@ import type { Database } from "../../../src/database/types.js";
 import { waitForDeferredTasks } from "../../../src/deferred-tasks.js";
 import { publishRedirectArtifacts } from "../../../src/redirects/artifacts.js";
 import { invalidateRedirectCache } from "../../../src/redirects/cache.js";
+import { runWithContext } from "../../../src/request-context.js";
+import { getSiteSettings, setSiteSettings } from "../../../src/settings/index.js";
 import { setupTestDatabase, teardownTestDatabase } from "../../utils/test-db.js";
 
 type MiddlewareContext = Parameters<typeof onRequest>[0];
@@ -724,6 +726,32 @@ describe("redirect middleware — responses the route cache stores", () => {
 		expect(selects).toBe(1);
 	});
 
+	it("restores the outer settings tracker after a nested cacheable render", async () => {
+		const cache = storingRouteCache();
+		const outerReads: string[] = [];
+
+		await runWithContext(
+			{
+				editMode: false,
+				routeCacheFill: true,
+				siteSettings: { onRead: (version) => outerReads.push(version) },
+			},
+			async () => {
+				const { context } = buildContext({ pathname: "/page", cache });
+				await runMiddleware(context, async () => {
+					await setSiteSettings({ title: "updated" }, db);
+					await getSiteSettings();
+					return new Response("page");
+				});
+
+				await getSiteSettings();
+			},
+		);
+
+		expect(outerReads).toHaveLength(1);
+		expect(cache.set).toHaveBeenCalledWith(false);
+	});
+
 	it("does not read the database for a render the route cache will not store", async () => {
 		await warm();
 		await repo.create({ source: "/page", destination: "/moved", type: 301 });
diff --git a/packages/core/tests/unit/astro/request-context-route-cache.test.ts b/packages/core/tests/unit/astro/request-context-route-cache.test.ts
index f42e9f602e..e8969219b8 100644
--- a/packages/core/tests/unit/astro/request-context-route-cache.test.ts
+++ b/packages/core/tests/unit/astro/request-context-route-cache.test.ts
@@ -42,6 +42,7 @@ import type { Database } from "../../../src/database/types.js";
 import { __setObjectCacheBackendForTests, cachedQuery } from "../../../src/object-cache/index.js";
 import { generatePreviewToken } from "../../../src/preview/tokens.js";
 import { getEmDashEntry } from "../../../src/query.js";
+import { requestCached } from "../../../src/request-cache.js";
 import { getRequestContext, runWithContext } from "../../../src/request-context.js";
 import { createPostFixture } from "../../utils/fixtures.js";
 import { setupTestDatabaseWithCollections, teardownTestDatabase } from "../../utils/test-db.js";
@@ -84,6 +85,20 @@ afterEach(() => {
 });
 
 describe("route-cache request context", () => {
+	it("reuses warmed reads when a cache-fill render re-enters for a rewrite", async () => {
+		const context = buildContext({ cache: { enabled: true, set: vi.fn() } });
+		const read = vi.fn(async () => "layout data");
+		const response = await onRequest(context, async () => {
+			await requestCached("layout", read);
+			return onRequest(
+				buildContext({ pathname: "/404", cache: context.cache }),
+				async () => new Response(await requestCached("layout", read)),
+			);
+		});
+		expect(await response.text()).toBe("layout data");
+		expect(read).toHaveBeenCalledOnce();
+	});
+
 	it("marks anonymous production cache renders as route-cache fills", async () => {
 		const cache = { enabled: true, set: vi.fn() };
 		const context = buildContext({ cache });