diff --git a/.changeset/fix-advanced-routing-404-fallback.md b/.changeset/fix-advanced-routing-404-fallback.md
new file mode 100644
index 000000000000..4ec812e69c1b
--- /dev/null
+++ b/.changeset/fix-advanced-routing-404-fallback.md
@@ -0,0 +1,5 @@
+---
+'astro': patch
+---
+
+Fixes a bug where `experimental.advancedRouting` with `astro/hono` handlers threw `TypeError: Cannot read properties of undefined (reading 'route')` for unmatched routes instead of rendering the custom 404 page.
diff --git a/packages/astro/src/core/fetch/fetch-state.ts b/packages/astro/src/core/fetch/fetch-state.ts
index afbbfc5eb552..3b531477e8c4 100644
--- a/packages/astro/src/core/fetch/fetch-state.ts
+++ b/packages/astro/src/core/fetch/fetch-state.ts
@@ -15,7 +15,6 @@ import { AstroCookies } from '../cookies/index.js';
 import { type Pipeline, Slots } from '../render/index.js';
 import {
 	ASTRO_GENERATOR,
-	DEFAULT_404_COMPONENT,
 	fetchStateSymbol,
 	originPathnameSymbol,
 	pipelineSymbol,
@@ -36,7 +35,7 @@ import { Rewrites } from '../rewrites/handler.js';
 import { isRoute404or500, isRouteServerIsland } from '../routing/match.js';
 import { normalizeUrl } from '../util/normalized-url.js';
 import { getOriginPathname, setOriginPathname } from '../routing/rewrite.js';
-import { routeHasHtmlExtension } from '../routing/helpers.js';
+import { getCustom404Route, routeHasHtmlExtension } from '../routing/helpers.js';
 import type { ResolvedRenderOptions } from '../app/base.js';
 import { getRenderOptions } from '../app/render-options.js';
 import { getFirstForwardedValue, validateForwardedHeaders } from '../app/validate-headers.js';
@@ -820,9 +819,14 @@ export class FetchState implements AstroFetchState {
 
 		// Fall back to a 404 route so middleware can still run.
 		if (!this.routeData) {
-			this.routeData = pipeline.manifestData.routes.find(
-				(route) => route.component === '404.astro' || route.component === DEFAULT_404_COMPONENT,
-			);
+			const custom404 = getCustom404Route(pipeline.manifestData);
+			// Only use SSR 404 routes here. Prerendered 404 pages are already
+			// built to static HTML, so the pipeline can't render them at
+			// runtime. Leaving routeData unset lets the error handler serve
+			// the pre-built page from disk instead.
+			if (custom404 && !custom404.prerender) {
+				this.routeData = custom404;
+			}
 		}
 		if (!this.routeData) {
 			pipeline.logger.debug('router', "Astro hasn't found routes that match " + this.request.url);
diff --git a/packages/astro/test/units/fetch/index.test.ts b/packages/astro/test/units/fetch/index.test.ts
index 9f2d6fb33409..3741e1b15d4f 100644
--- a/packages/astro/test/units/fetch/index.test.ts
+++ b/packages/astro/test/units/fetch/index.test.ts
@@ -79,6 +79,16 @@ describe('FetchState (astro/fetch)', () => {
 		assert.equal(state.routeData!.route, '/[b_ssr]');
 		assert.equal(state.routeData!.prerender, false);
 	});
+
+	it('falls back to the 404 route when no route matches', () => {
+		const notFoundPage = createPage(simplePage, { route: '/404' });
+		const app = createTestApp([createPage(simplePage, { route: '/' }), notFoundPage]);
+		const request = stampApp(new Request('http://example.com/does-not-exist'), app);
+		const state = new FetchState(request);
+
+		assert.ok(state.routeData, 'routeData should fall back to the 404 route');
+		assert.equal(state.routeData!.route, '/404');
+	});
 });
 
 // #endregion
@@ -238,6 +248,24 @@ describe('pages()', () => {
 		assert.match(text, /<h1>Hello<\/h1>/);
 	});
 
+	it('renders the 404 page for unmatched routes instead of throwing', async () => {
+		const notFoundPage = createComponent((_result: any, _props: any, _slots: any) => {
+			return render`<h1>Not Found</h1>`;
+		});
+		const app = createTestApp([
+			createPage(simplePage, { route: '/' }),
+			createPage(notFoundPage, { route: '/404' }),
+		]);
+		const request = stampApp(new Request('http://example.com/does-not-exist'), app);
+		const state = new FetchState(request);
+
+		const response = await pages(state);
+
+		assert.equal(response.status, 404);
+		const text = await response.text();
+		assert.match(text, /<h1>Not Found<\/h1>/);
+	});
+
 	it('renders an endpoint', async () => {
 		const app = createTestApp([
 			createEndpoint(