diff --git a/.changeset/modern-rooms-cry.md b/.changeset/modern-rooms-cry.md
new file mode 100644
index 000000000000..e7c983fcd9b6
--- /dev/null
+++ b/.changeset/modern-rooms-cry.md
@@ -0,0 +1,5 @@
+---
+'@astrojs/cloudflare': patch
+---
+
+Fixed a bug where a cascade of reloads would cause the page to crash during the first visit when building or developing with Cloudflare SSR in Astro v6 due to dependency loading issues.
diff --git a/packages/integrations/cloudflare/src/esbuild-plugin-astro-frontmatter.ts b/packages/integrations/cloudflare/src/esbuild-plugin-astro-frontmatter.ts
index 4a3e4039d67a..f9057dec69ad 100644
--- a/packages/integrations/cloudflare/src/esbuild-plugin-astro-frontmatter.ts
+++ b/packages/integrations/cloudflare/src/esbuild-plugin-astro-frontmatter.ts
@@ -1,4 +1,5 @@
 import { readFile } from 'node:fs/promises';
+import { dirname, isAbsolute, resolve } from 'node:path';
 import type { DepOptimizationConfig } from 'vite';
 
 const FRONTMATTER_RE = /^---\r?\n([\s\S]*?)\r?\n---/;
@@ -16,6 +17,8 @@ function replaceTopLevelReturns(code: string): string {
 	});
 }
 
+const ASTRO_FRONTMATTER_NAMESPACE = 'astro-frontmatter';
+
 // Not exposed as a type from Vite, so need to grab this way.
 type ESBuildPlugin = NonNullable<
 	NonNullable<DepOptimizationConfig['esbuildOptions']>['plugins']
@@ -25,47 +28,61 @@ type ESBuildPlugin = NonNullable<
  * An esbuild plugin that extracts frontmatter from .astro files during
  * dependency optimization scanning. This allows Vite to discover imports
  * in the server-side frontmatter code.
+ *
+ * This plugin uses an `onResolve` handler to intercept `.astro` files before
+ * Vite's built-in `vite:dep-scan` plugin routes them to the `html` namespace.
+ * Without this, Vite's scanner only extracts `<script>` tags from `.astro`
+ * files, completely missing frontmatter imports (which is where SSR-side
+ * dependencies like `zod`, `nanostores`, `astro:transitions`, etc. live).
  */
 export function astroFrontmatterScanPlugin(): ESBuildPlugin {
 	return {
 		name: 'astro-frontmatter-scan',
 		setup(build) {
-			// Scope to the "file" namespace so that .astro files resolved into the
-			// "html" namespace (e.g. when a .ts file default-imports a component)
-			// fall through to Vite's built-in html-type handler, which appends
-			// `export default {}` and avoids "No matching export" errors.
-			build.onLoad({ filter: /\.astro$/, namespace: 'file' }, async (args) => {
-				try {
-					const code = await readFile(args.path, 'utf-8');
+			// Intercept .astro file resolution to route them through our namespace
+			// before Vite's `vite:dep-scan` plugin puts them in the `html` namespace.
+			// In esbuild, plugins are processed in order and the first `onResolve`
+			// match wins. Since user plugins (including this one) are registered before
+			// Vite's scanner plugin, this handler takes priority.
+			build.onResolve({ filter: /\.astro$/ }, (args) => {
+				// Only intercept files in the default namespace. Files already in a
+				// custom namespace are either already claimed or are re-entry points
+				// that should not be processed again.
+				if (args.namespace !== 'file' && args.namespace !== '' && args.namespace !== undefined) {
+					return undefined;
+				}
+				const resolvedPath = isAbsolute(args.path)
+					? args.path
+					: resolve(args.resolveDir, args.path);
+				return { path: resolvedPath, namespace: ASTRO_FRONTMATTER_NAMESPACE };
+			});
 
-					// Extract frontmatter content between --- markers
-					const frontmatterMatch = FRONTMATTER_RE.exec(code);
-					if (frontmatterMatch) {
-						// Replace `return` with `throw` to avoid esbuild's "Top-level return" error during scanning.
-						// This aligns with Astro's core compiler logic for frontmatter error handling.
-						// See: packages/astro/src/vite-plugin-astro/compile.ts
-						const contents = replaceTopLevelReturns(frontmatterMatch[1]);
+			build.onLoad(
+				{ filter: /\.astro$/, namespace: ASTRO_FRONTMATTER_NAMESPACE },
+				async (args) => {
+					try {
+						const code = await readFile(args.path, 'utf-8');
 
-						// Append `export default {}` so that default imports of .astro files
-						// (e.g. `import MyComponent from './MyComponent.astro'`) resolve correctly
-						// during the dep scan. Without this, .astro files loaded in the `html`
-						// namespace (when imported from .ts files) would have no default export,
-						// causing esbuild to fail with "No matching export for import 'default'".
-						return {
-							contents: contents + '\nexport default {}',
-							loader: 'ts',
-						};
+						const frontmatterMatch = FRONTMATTER_RE.exec(code);
+						if (frontmatterMatch) {
+							const contents = replaceTopLevelReturns(frontmatterMatch[1]);
+							return {
+								contents: contents + '\nexport default {}',
+								loader: 'ts',
+								resolveDir: dirname(args.path),
+							};
+						}
+					} catch {
+						// Ignore read errors
 					}
-				} catch {
-					// Ignore read errors
-				}
 
-				// No frontmatter or read error, return empty with a default export
-				return {
-					contents: 'export default {}',
-					loader: 'ts',
-				};
-			});
+					return {
+						contents: 'export default {}',
+						loader: 'ts',
+						resolveDir: dirname(args.path),
+					};
+				},
+			);
 		},
 	};
 }
diff --git a/packages/integrations/cloudflare/src/index.ts b/packages/integrations/cloudflare/src/index.ts
index a8dec400e36a..d0a4e80037cb 100644
--- a/packages/integrations/cloudflare/src/index.ts
+++ b/packages/integrations/cloudflare/src/index.ts
@@ -286,6 +286,11 @@ export default function createIntegration({
 													'astro/jsx-runtime',
 													'astro/app/entrypoint/dev',
 													'astro/virtual-modules/middleware.js',
+													'astro/virtual-modules/transitions.js',
+													'astro/virtual-modules/transitions-router.js',
+													'astro/virtual-modules/transitions-types.js',
+													'astro/virtual-modules/transitions-events.js',
+													'astro/virtual-modules/transitions-swap-functions.js',
 													...(isAstroPrismPackageInstalled ? prismFiles : []),
 												],
 												exclude: [
@@ -296,6 +301,7 @@ export default function createIntegration({
 													'virtual:@astrojs/*',
 													'@astrojs/starlight',
 												],
+												ignoreOutdatedRequests: true,
 												esbuildOptions: {
 													// Suppress Vite's `createRequire(import.meta.url)` banner to work around
 													// https://github.com/vitejs/vite/issues/22004 — Vite's SSR transform
diff --git a/packages/integrations/cloudflare/test/dev-ssr-optimization.test.ts b/packages/integrations/cloudflare/test/dev-ssr-optimization.test.ts
new file mode 100644
index 000000000000..4d9c9e4a3996
--- /dev/null
+++ b/packages/integrations/cloudflare/test/dev-ssr-optimization.test.ts
@@ -0,0 +1,145 @@
+import * as assert from 'node:assert/strict';
+import { Writable } from 'node:stream';
+import { after, before, describe, it } from 'node:test';
+import * as cheerio from 'cheerio';
+import { AstroLogger } from '../../../astro/dist/core/logger/core.js';
+import cloudflare from '../dist/index.js';
+import { astroFrontmatterScanPlugin } from '../dist/esbuild-plugin-astro-frontmatter.js';
+import { type DevServer, type Fixture, loadFixture } from './test-utils.ts';
+
+describe('Cloudflare SSR Optimization', () => {
+	// Verifies that the Cloudflare integration's SSR optimization plugin
+	// correctly pre-registers critical virtual modules and configures Vite to handle cascading re-optimizations gracefully,
+	// preventing crashes during development when using features like View Transitions.
+  async function captureEnvironmentPlugin(): Promise<any> {
+    const integration = cloudflare({});
+    const capturedPlugins: any[] = [];
+
+    await integration.hooks['astro:config:setup']?.({
+      command: 'dev',
+      isRestart: false,
+      config: {
+        root: new URL('file:///tmp/'),
+        srcDir: new URL('file:///tmp/src/'),
+        session: { driver: 'memory' },
+      } as any,
+      updateConfig: (cfg: any) => {
+        const plugins = [cfg?.vite?.plugins ?? []].flat(Number.POSITIVE_INFINITY);
+        capturedPlugins.push(...plugins.filter(Boolean));
+      },
+      addWatchFile: () => {},
+      logger: { info: () => {}, warn: () => {}, error: () => {}, debug: () => {} } as any,
+    } as any);
+
+    return capturedPlugins.find((p: any) => p?.name === '@astrojs/cloudflare:environment') ?? null;
+  }
+
+	// Note: These tests are designed to run in a Node environment and may not be compatible with browser-based testing frameworks.
+  describe('Astro Frontmatter Scanner', () => {
+    it('registers an onResolve handler to prioritize .astro file interception and dependency discovery', () => {
+      const plugin = astroFrontmatterScanPlugin();
+      const resolvers: Array<{ filter: RegExp }> = [];
+
+      void plugin.setup({
+        onResolve(options: { filter: RegExp }, _callback: (...args: unknown[]) => unknown) {
+          resolvers.push(options);
+        },
+        onLoad(_options: any, _callback: (...args: unknown[]) => unknown) {},
+      } as any);
+
+      const hasAstroResolver = resolvers.some((r) => r.filter.test('Component.astro'));
+      assert.equal(hasAstroResolver, true);
+    });
+  });
+
+  const TRANSITIONS_MODULES = [
+    'astro/virtual-modules/transitions.js',
+    'astro/virtual-modules/transitions-router.js',
+    'astro/virtual-modules/transitions-types.js',
+    'astro/virtual-modules/transitions-events.js',
+    'astro/virtual-modules/transitions-swap-functions.js',
+  ] as const;
+
+  // SSR environment in which critical virtual modules are pre-registered and reload resilience is configured
+  // to ensure they are correctly injected.
+  describe('Vite Environment Configuration', () => {
+    let envPlugin: any;
+
+    before(async () => {
+      envPlugin = await captureEnvironmentPlugin();
+    });
+
+    for (const envName of ['astro', 'ssr', 'prerender'] as const) {
+      it(`explicitly includes View Transitions virtual modules in "${envName}" environment to prevent runtime discovery`, () => {
+        const config = envPlugin?.configEnvironment(envName, {});
+        const include: string[] = config?.optimizeDeps?.include ?? [];
+        const missing = TRANSITIONS_MODULES.filter((m) => !include.includes(m));
+        assert.deepEqual(missing, [], `Missing virtual modules in "${envName}": ${missing.join(', ')}`);
+      });
+
+      it(`enables ignoreOutdatedRequests for "${envName}" environment to prevent crashes during cascading re-optimization`, () => {
+        const config = envPlugin?.configEnvironment(envName, {});
+        assert.equal(config?.optimizeDeps?.ignoreOutdatedRequests, true);
+      });
+    }
+  });
+
+  // Verify that the dev server remains stable and correctly handles SSR optimizations without crashing
+	// even when features like View Transitions trigger multiple optimization cycles.
+  describe('Dev Server Runtime Behavior', () => {
+    let fixture: Fixture;
+    let devServer: DevServer;
+    const logs: string[] = [];
+
+    before(async () => {
+      fixture = await loadFixture({
+        root: './fixtures/dev-ssr-optimization/',
+      });
+
+      const logger = new AstroLogger({
+        level: 'warn',
+        destination: new Writable({
+          objectMode: true,
+          write(event, _, callback) {
+            logs.push(event.message);
+            callback();
+          },
+        }),
+      });
+
+      devServer = await fixture.startDevServer({
+        // @ts-expect-error: logger is @internal
+        logger,
+      });
+
+      // initial request to trigger optimization and potential re-optimization cycles
+      await fixture.fetch('/');
+    });
+
+    after(async () => {
+      await devServer.stop();
+    });
+
+    it('successfully serves the initial request without triggering fatal optimization errors', async () => {
+      const res = await fixture.fetch('/');
+      assert.equal(res.status, 200);
+    });
+
+    it('maintains stability across multiple requests and handles in-place restarts', async () => {
+      const res = await fixture.fetch('/');
+      assert.equal(res.status, 200);
+    });
+
+    it('suppresses "The file does not exist" errors by handling stale chunk references gracefully', () => {
+      const staleChunkErrors = logs.filter((msg) => msg.includes('The file does not exist'));
+      assert.equal(staleChunkErrors.length, 0);
+    });
+
+    it('ensures correct server-side rendering of pages utilizing View Transitions', async () => {
+      const res = await fixture.fetch('/');
+      const html = await res.text();
+      const $ = cheerio.load(html);
+      assert.equal($('#content').text(), 'OK');
+    });
+  });
+});
diff --git a/packages/integrations/cloudflare/test/fixtures/dev-ssr-optimization/astro.config.mjs b/packages/integrations/cloudflare/test/fixtures/dev-ssr-optimization/astro.config.mjs
new file mode 100644
index 000000000000..95234c069ab7
--- /dev/null
+++ b/packages/integrations/cloudflare/test/fixtures/dev-ssr-optimization/astro.config.mjs
@@ -0,0 +1,11 @@
+import cloudflare from '@astrojs/cloudflare';
+import { defineConfig } from 'astro/config';
+
+export default defineConfig({
+	adapter: cloudflare({
+		platformProxy: {
+			enabled: true,
+		},
+	}),
+	output: 'server',
+});
diff --git a/packages/integrations/cloudflare/test/fixtures/dev-ssr-optimization/package.json b/packages/integrations/cloudflare/test/fixtures/dev-ssr-optimization/package.json
new file mode 100644
index 000000000000..27b47e213fd4
--- /dev/null
+++ b/packages/integrations/cloudflare/test/fixtures/dev-ssr-optimization/package.json
@@ -0,0 +1,12 @@
+{
+  "name": "@test/cloudflare-dev-ssr-optimization",
+  "version": "0.0.0",
+  "private": true,
+  "dependencies": {
+    "@astrojs/cloudflare": "workspace:*",
+    "astro": "workspace:*"
+  },
+  "devDependencies": {
+    "wrangler": "^4.83.0"
+  }
+}
diff --git a/packages/integrations/cloudflare/test/fixtures/dev-ssr-optimization/src/components/Counter.svelte b/packages/integrations/cloudflare/test/fixtures/dev-ssr-optimization/src/components/Counter.svelte
new file mode 100644
index 000000000000..cbfe49244a77
--- /dev/null
+++ b/packages/integrations/cloudflare/test/fixtures/dev-ssr-optimization/src/components/Counter.svelte
@@ -0,0 +1,5 @@
+<script>
+	let count = $state(0);
+</script>
+
+<button onclick={() => count++}>Count: {count}</button>
diff --git a/packages/integrations/cloudflare/test/fixtures/dev-ssr-optimization/src/pages/index.astro b/packages/integrations/cloudflare/test/fixtures/dev-ssr-optimization/src/pages/index.astro
new file mode 100644
index 000000000000..396d2d384b6d
--- /dev/null
+++ b/packages/integrations/cloudflare/test/fixtures/dev-ssr-optimization/src/pages/index.astro
@@ -0,0 +1,13 @@
+---
+import { ClientRouter } from 'astro:transitions';
+---
+<html lang="en">
+	<head>
+		<meta charset="utf-8" />
+		<title>Dev SSR Optimization Test</title>
+		<ClientRouter />
+	</head>
+	<body>
+		<div id="content">OK</div>
+	</body>
+</html>
diff --git a/pnpm-lock.yaml b/pnpm-lock.yaml
index 5f017934c0d5..a6624090c0cb 100644
--- a/pnpm-lock.yaml
+++ b/pnpm-lock.yaml
@@ -4591,6 +4591,19 @@ importers:
         specifier: workspace:*
         version: link:../../../../../astro
 
+  packages/integrations/cloudflare/test/fixtures/dev-ssr-optimization:
+    dependencies:
+      '@astrojs/cloudflare':
+        specifier: workspace:*
+        version: link:../../..
+      astro:
+        specifier: workspace:*
+        version: link:../../../../../astro
+    devDependencies:
+      wrangler:
+        specifier: ^4.83.0
+        version: 4.83.0(@cloudflare/workers-types@4.20260228.0)
+
   packages/integrations/cloudflare/test/fixtures/external-image-service:
     dependencies:
       '@astrojs/cloudflare':