diff --git a/packages/astro/src/core/app/index.ts b/packages/astro/src/core/app/index.ts
index 566d0c60d..6b92bed92 100644
--- a/packages/astro/src/core/app/index.ts
+++ b/packages/astro/src/core/app/index.ts
@@ -9,7 +9,7 @@ import type {
 import type { SinglePageBuiltModule } from '../build/types';
 import { getSetCookiesFromResponse } from '../cookies/index.js';
 import { consoleLogDestination } from '../logger/console.js';
-import { error, type LogOptions } from '../logger/core.js';
+import { error, type LogOptions, warn } from '../logger/core.js';
 import {
 	collapseDuplicateSlashes,
 	prependForwardSlash,
@@ -56,6 +56,8 @@ export class App {
 	};
 	#baseWithoutTrailingSlash: string;
 	#pipeline: SSRRoutePipeline;
+	#onRequest: MiddlewareEndpointHandler | undefined;
+	#middlewareLoaded: boolean;
 
 	constructor(manifest: SSRManifest, streaming = true) {
 		this.#manifest = manifest;
@@ -65,6 +67,7 @@ export class App {
 		this.#routeDataToRouteInfo = new Map(manifest.routes.map((route) => [route.routeData, route]));
 		this.#baseWithoutTrailingSlash = removeTrailingForwardSlash(this.#manifest.base);
 		this.#pipeline = new SSRRoutePipeline(this.#createEnvironment(streaming));
+		this.#middlewareLoaded = false;
 	}
 
 	set setManifest(newManifest: SSRManifest) {
@@ -128,7 +131,21 @@ export class App {
 		if (!routeData || routeData.prerender) return undefined;
 		return routeData;
 	}
+
+	async #getOnRequest() {
+		if (this.#manifest.middlewareEntryPoint && !this.#middlewareLoaded) {
+			try {
+				const middleware = await import(this.#manifest.middlewareEntryPoint);
+				this.#pipeline.setMiddlewareFunction(middleware.onRequest as MiddlewareEndpointHandler);
+			} catch (e) {
+				warn(this.#logging, 'SSR', "Couldn't load the middleware entry point");
+			}
+		}
+		this.#middlewareLoaded = true;
+	}
+
 	async render(request: Request, routeData?: RouteData, locals?: object): Promise<Response> {
+		await this.#getOnRequest();
 		// Handle requests with duplicate slashes gracefully by cloning with a cleaned-up request URL
 		if (request.url !== collapseDuplicateSlashes(request.url)) {
 			request = new Request(collapseDuplicateSlashes(request.url), request);
@@ -156,10 +173,6 @@ export class App {
 		);
 		let response;
 		try {
-			// NOTE: ideally we could set the middleware function just once, but we don't have the infrastructure to that yet
-			if (mod.onRequest) {
-				this.#pipeline.setMiddlewareFunction(mod.onRequest as MiddlewareEndpointHandler);
-			}
 			response = await this.#pipeline.renderRoute(renderContext, pageModule);
 		} catch (err: any) {
 			if (err instanceof EndpointNotFoundError) {
diff --git a/packages/astro/src/core/app/types.ts b/packages/astro/src/core/app/types.ts
index 8812d2c44..faeb9377e 100644
--- a/packages/astro/src/core/app/types.ts
+++ b/packages/astro/src/core/app/types.ts
@@ -49,6 +49,7 @@ export type SSRManifest = {
 	componentMetadata: SSRResult['componentMetadata'];
 	pageModule?: SinglePageBuiltModule;
 	pageMap?: Map<ComponentPath, ImportComponentInstance>;
+	middlewareEntryPoint: string | undefined;
 };
 
 export type SerializedSSRManifest = Omit<
diff --git a/packages/astro/src/core/build/buildPipeline.ts b/packages/astro/src/core/build/buildPipeline.ts
index 5815fa5f5..ea6e9ecf4 100644
--- a/packages/astro/src/core/build/buildPipeline.ts
+++ b/packages/astro/src/core/build/buildPipeline.ts
@@ -77,6 +77,13 @@ export class BuildPipeline extends Pipeline {
 		return this.#manifest;
 	}
 
+	async retrieveMiddlewareFunction() {
+		if (this.#internals.middlewareEntryPoint) {
+			const middleware = await import(this.#internals.middlewareEntryPoint.toString());
+			this.setMiddlewareFunction(middleware.onRequest);
+		}
+	}
+
 	/**
 	 * The SSR build emits two important files:
 	 * - dist/server/manifest.mjs
diff --git a/packages/astro/src/core/build/generate.ts b/packages/astro/src/core/build/generate.ts
index 224b96b63..73bb4a40f 100644
--- a/packages/astro/src/core/build/generate.ts
+++ b/packages/astro/src/core/build/generate.ts
@@ -10,7 +10,6 @@ import type {
 	ComponentInstance,
 	GetStaticPathsItem,
 	ImageTransform,
-	MiddlewareEndpointHandler,
 	RouteData,
 	RouteType,
 	SSRError,
@@ -138,6 +137,7 @@ export async function generatePages(opts: StaticBuildOptions, internals: BuildIn
 		);
 	}
 	const buildPipeline = new BuildPipeline(opts, internals, manifest);
+	await buildPipeline.retrieveMiddlewareFunction();
 	const outFolder = ssr
 		? opts.settings.config.build.server
 		: getOutDirWithinCwd(opts.settings.config.outDir);
@@ -248,10 +248,6 @@ async function generatePage(
 		.reduce(mergeInlineCss, []);
 
 	const pageModulePromise = ssrEntry.page;
-	const onRequest = ssrEntry.onRequest;
-	if (onRequest) {
-		pipeline.setMiddlewareFunction(onRequest as MiddlewareEndpointHandler);
-	}
 
 	if (!pageModulePromise) {
 		throw new Error(
@@ -612,5 +608,8 @@ export function createBuildManifest(
 			? new URL(settings.config.base, settings.config.site).toString()
 			: settings.config.site,
 		componentMetadata: internals.componentMetadata,
+		middlewareEntryPoint: internals.middlewareEntryPoint
+			? internals.middlewareEntryPoint.toString()
+			: undefined,
 	};
 }
diff --git a/packages/astro/src/core/build/plugins/plugin-manifest.ts b/packages/astro/src/core/build/plugins/plugin-manifest.ts
index a7b254554..1364ebf1e 100644
--- a/packages/astro/src/core/build/plugins/plugin-manifest.ts
+++ b/packages/astro/src/core/build/plugins/plugin-manifest.ts
@@ -93,14 +93,19 @@ export function pluginManifest(
 				}
 
 				const manifest = await createManifest(options, internals);
+				const shouldPassMiddlewareEntryPoint =
+					// TODO: remove in Astro 4.0
+					options.settings.config.build.excludeMiddleware ||
+					options.settings.adapter?.adapterFeatures?.edgeMiddleware;
 				await runHookBuildSsr({
 					config: options.settings.config,
 					manifest,
 					logging: options.logging,
 					entryPoints: internals.entryPoints,
-					middlewareEntryPoint: internals.middlewareEntryPoint,
+					middlewareEntryPoint: shouldPassMiddlewareEntryPoint
+						? internals.middlewareEntryPoint
+						: undefined,
 				});
-				// TODO: use the manifest entry chunk instead
 				const code = injectManifest(manifest, internals.manifestEntryChunk);
 				mutate(internals.manifestEntryChunk, 'server', code);
 			},
@@ -232,6 +237,10 @@ function buildManifest(
 		// Set this to an empty string so that the runtime knows not to try and load this.
 		entryModules[BEFORE_HYDRATION_SCRIPT_ID] = '';
 	}
+	const isEdgeMiddleware =
+		// TODO: remove in Astro 4.0
+		settings.config.build.excludeMiddleware ||
+		settings.adapter?.adapterFeatures?.edgeMiddleware;
 
 	const ssrManifest: SerializedSSRManifest = {
 		adapterName: opts.settings.adapter?.name ?? '',
@@ -245,6 +254,7 @@ function buildManifest(
 		clientDirectives: Array.from(settings.clientDirectives),
 		entryModules,
 		assets: staticFiles.map(prefixAssetPath),
+		middlewareEntryPoint: !isEdgeMiddleware ? internals.middlewareEntryPoint?.toString() : undefined,
 	};
 
 	return ssrManifest;
diff --git a/packages/astro/src/core/build/plugins/plugin-middleware.ts b/packages/astro/src/core/build/plugins/plugin-middleware.ts
index 5ed532d5e..7c945740c 100644
--- a/packages/astro/src/core/build/plugins/plugin-middleware.ts
+++ b/packages/astro/src/core/build/plugins/plugin-middleware.ts
@@ -4,6 +4,7 @@ import { addRollupInput } from '../add-rollup-input.js';
 import type { BuildInternals } from '../internal';
 import type { AstroBuildPlugin } from '../plugin';
 import type { StaticBuildOptions } from '../types';
+import { getOutputDirectory } from '../../../prerender/utils.js';
 
 export const MIDDLEWARE_MODULE_ID = '@astro-middleware';
 
@@ -56,8 +57,9 @@ export function vitePluginMiddleware(
 				if (chunk.type === 'asset') {
 					continue;
 				}
-				if (chunk.fileName === 'middleware.mjs' && opts.settings.config.build.excludeMiddleware) {
-					internals.middlewareEntryPoint = new URL(chunkName, opts.settings.config.build.server);
+				if (chunk.fileName === 'middleware.mjs') {
+					const outputDirectory = getOutputDirectory(opts.settings.config);
+					internals.middlewareEntryPoint = new URL(chunkName, outputDirectory);
 				}
 			}
 		},
diff --git a/packages/astro/src/core/build/types.ts b/packages/astro/src/core/build/types.ts
index 472dc4b34..35451cacb 100644
--- a/packages/astro/src/core/build/types.ts
+++ b/packages/astro/src/core/build/types.ts
@@ -4,7 +4,6 @@ import type {
 	AstroSettings,
 	ComponentInstance,
 	ManifestData,
-	MiddlewareHandler,
 	RouteData,
 	RuntimeMode,
 	SSRLoadedRenderer,
@@ -52,7 +51,6 @@ export interface SinglePageBuiltModule {
 	/**
 	 * The `onRequest` hook exported by the middleware
 	 */
-	onRequest?: MiddlewareHandler<unknown>;
 	renderers: SSRLoadedRenderer[];
 }
 
diff --git a/packages/astro/src/core/redirects/component.ts b/packages/astro/src/core/redirects/component.ts
index d10cae4fe..93b1aa732 100644
--- a/packages/astro/src/core/redirects/component.ts
+++ b/packages/astro/src/core/redirects/component.ts
@@ -12,6 +12,5 @@ export const RedirectComponentInstance: ComponentInstance = {
 
 export const RedirectSinglePageBuiltModule: SinglePageBuiltModule = {
 	page: () => Promise.resolve(RedirectComponentInstance),
-	onRequest: (ctx, next) => next(),
 	renderers: [],
 };
diff --git a/packages/astro/src/vite-plugin-astro-server/plugin.ts b/packages/astro/src/vite-plugin-astro-server/plugin.ts
index f7f7b0068..374f31fec 100644
--- a/packages/astro/src/vite-plugin-astro-server/plugin.ts
+++ b/packages/astro/src/vite-plugin-astro-server/plugin.ts
@@ -99,5 +99,6 @@ export function createDevelopmentManifest(settings: AstroSettings): SSRManifest
 			? new URL(settings.config.base, settings.config.site).toString()
 			: settings.config.site,
 		componentMetadata: new Map(),
+		middlewareEntryPoint: undefined,
 	};
 }
diff --git a/packages/astro/test/fixtures/middleware-dev/src/middleware.js b/packages/astro/test/fixtures/middleware-dev/src/middleware.js
index 854c997c1..eeb902fb8 100644
--- a/packages/astro/test/fixtures/middleware-dev/src/middleware.js
+++ b/packages/astro/test/fixtures/middleware-dev/src/middleware.js
@@ -18,18 +18,20 @@ const first = defineMiddleware(async (context, next) => {
 		return new Response(JSON.stringify(object), {
 			headers: response.headers,
 		});
-	} else if(context.url.pathname === '/clone') {
+	} else if (context.url.pathname === '/clone') {
 		const response = await next();
 		const newResponse = response.clone();
 		const /** @type {string} */ html = await newResponse.text();
 		const newhtml = html.replace('<h1>testing</h1>', '<h1>it works</h1>');
 		return new Response(newhtml, { status: 200, headers: response.headers });
 	} else {
-		if(context.url.pathname === '/') {
+		if (context.url.pathname === '/') {
 			context.cookies.set('foo', 'bar');
 		}
 
-		context.locals.name = 'bar';
+		context.locals = {
+			name: 'bar',
+		};
 	}
 	return await next();
 });
diff --git a/packages/astro/test/fixtures/middleware-dev/src/pages/404.astro b/packages/astro/test/fixtures/middleware-dev/src/pages/404.astro
new file mode 100644
index 000000000..ea85d240c
--- /dev/null
+++ b/packages/astro/test/fixtures/middleware-dev/src/pages/404.astro
@@ -0,0 +1,6 @@
+---
+const name = Astro.locals.name;
+---
+
+<title>Error</title>
+<p>{name}</p>
diff --git a/packages/astro/test/middleware.test.js b/packages/astro/test/middleware.test.js
index 3796a341f..b09c686f4 100644
--- a/packages/astro/test/middleware.test.js
+++ b/packages/astro/test/middleware.test.js
@@ -211,6 +211,16 @@ describe('Middleware API in PROD mode, SSR', () => {
 		expect(text.includes('REDACTED')).to.be.true;
 	});
 
+	it('should correctly call the middleware function for 404', async () => {
+		const app = await fixture.loadTestAdapterApp();
+		const request = new Request('http://example.com/funky-url');
+		const routeData = app.match(request, { matchNotFound: true });
+		const response = await app.render(request, routeData);
+		const text = await response.text();
+		expect(text.includes('Error')).to.be.true;
+		expect(text.includes('bar')).to.be.true;
+	});
+	
 	it('the integration should receive the path to the middleware', async () => {
 		fixture = await loadFixture({
 			root: './fixtures/middleware-dev/',
@@ -219,10 +229,8 @@ describe('Middleware API in PROD mode, SSR', () => {
 				excludeMiddleware: true,
 			},
 			adapter: testAdapter({
-				setEntryPoints(entryPointsOrMiddleware) {
-					if (entryPointsOrMiddleware instanceof URL) {
-						middlewarePath = entryPointsOrMiddleware;
-					}
+				setMiddlewareEntryPoint(entryPointsOrMiddleware) {
+					middlewarePath = entryPointsOrMiddleware;
 				},
 			}),
 		});
@@ -237,6 +245,7 @@ describe('Middleware API in PROD mode, SSR', () => {
 			throw e;
 		}
 	});
+
 });
 
 describe('Middleware with tailwind', () => {
diff --git a/packages/astro/test/test-adapter.js b/packages/astro/test/test-adapter.js
index 67058023d..0090b6d9d 100644
--- a/packages/astro/test/test-adapter.js
+++ b/packages/astro/test/test-adapter.js
@@ -5,7 +5,13 @@ import { viteID } from '../dist/core/util.js';
  * @returns {import('../src/@types/astro').AstroIntegration}
  */
 export default function (
-	{ provideAddress = true, extendAdapter, setEntryPoints = undefined, setRoutes = undefined } = {
+	{
+		provideAddress = true,
+		extendAdapter,
+		setEntryPoints = undefined,
+		setMiddlewareEntryPoint = undefined,
+		setRoutes = undefined,
+	} = {
 		provideAddress: true,
 	}
 ) {
@@ -86,7 +92,9 @@ export default function (
 			'astro:build:ssr': ({ entryPoints, middlewareEntryPoint }) => {
 				if (setEntryPoints) {
 					setEntryPoints(entryPoints);
-					setEntryPoints(middlewareEntryPoint);
+				}
+				if (setMiddlewareEntryPoint) {
+					setMiddlewareEntryPoint(middlewareEntryPoint);
 				}
 			},
 			'astro:build:done': ({ routes }) => {