diff --git a/.changeset/curly-mails-lie.md b/.changeset/curly-mails-lie.md
new file mode 100644
index 000000000000..70f57323fd3d
--- /dev/null
+++ b/.changeset/curly-mails-lie.md
@@ -0,0 +1,5 @@
+---
+'astro': patch
+---
+
+Fix dev routing for `server:defer` islands when adapters opt into handling prerendered routes in Astro core. Server island requests are now treated as prerender-handler eligible so prerendered pages using `prerenderEnvironment: 'node'` can load island content without `400` errors.
diff --git a/packages/astro/src/vite-plugin-astro-server/plugin.ts b/packages/astro/src/vite-plugin-astro-server/plugin.ts
index f4866f99b5a0..89ff91b5a53e 100644
--- a/packages/astro/src/vite-plugin-astro-server/plugin.ts
+++ b/packages/astro/src/vite-plugin-astro-server/plugin.ts
@@ -22,7 +22,7 @@ import { AstroError, AstroErrorData } from '../core/errors/index.js';
import type { Logger } from '../core/logger/core.js';
import { NOOP_MIDDLEWARE_FN } from '../core/middleware/noop-middleware.js';
import { createViteLoader } from '../core/module-loader/index.js';
-import { matchAllRoutes } from '../core/routing/match.js';
+import { isRouteServerIsland, matchAllRoutes } from '../core/routing/match.js';
import { resolveMiddlewareMode } from '../integrations/adapter-utils.js';
import { SERIALIZED_MANIFEST_ID } from '../manifest/serialized.js';
import type { AstroSettings } from '../types/astro.js';
@@ -176,7 +176,7 @@ export default function createVitePluginAstroServer({
const routesList = { routes: routes.map((r: any) => r.routeData) };
const matches = matchAllRoutes(pathname, routesList);
- if (!matches.some((route) => route.prerender)) {
+ if (!matches.some((route) => route.prerender || isRouteServerIsland(route))) {
return next();
}
diff --git a/packages/integrations/cloudflare/test/fixtures/prerender-node-env/src/components/DeferredIsland.astro b/packages/integrations/cloudflare/test/fixtures/prerender-node-env/src/components/DeferredIsland.astro
new file mode 100644
index 000000000000..406b874edfe6
--- /dev/null
+++ b/packages/integrations/cloudflare/test/fixtures/prerender-node-env/src/components/DeferredIsland.astro
@@ -0,0 +1 @@
+deferred island content
diff --git a/packages/integrations/cloudflare/test/fixtures/prerender-node-env/src/pages/index.astro b/packages/integrations/cloudflare/test/fixtures/prerender-node-env/src/pages/index.astro
index 92c69edf9b55..fb8441836b45 100644
--- a/packages/integrations/cloudflare/test/fixtures/prerender-node-env/src/pages/index.astro
+++ b/packages/integrations/cloudflare/test/fixtures/prerender-node-env/src/pages/index.astro
@@ -3,6 +3,7 @@ export const prerender = true;
import fs from 'node:fs';
import path from 'node:path';
+import DeferredIsland from '../components/DeferredIsland.astro';
const packageJsonPath = path.join(process.cwd(), 'package.json');
const packageJson = JSON.parse(fs.readFileSync(packageJsonPath, 'utf-8'));
@@ -20,5 +21,8 @@ const packageJson = JSON.parse(fs.readFileSync(packageJsonPath, 'utf-8'));
Prerendered
{packageJson.name}
+
+ loading...
+