diff --git a/.changeset/dry-suns-protect.md b/.changeset/dry-suns-protect.md
new file mode 100644
index 0000000000000..1204142622e5e
--- /dev/null
+++ b/.changeset/dry-suns-protect.md
@@ -0,0 +1,5 @@
+---
+"astro": patch
+---
+
+Fixes a regression where the dev server was returning a 404 when hitting an endpoint, when the app was configured with `trailingSlash: "always"`
diff --git a/packages/astro/src/core/routing/manifest/create.ts b/packages/astro/src/core/routing/manifest/create.ts
index 804cacc83fde5..28c842a59f7b9 100644
--- a/packages/astro/src/core/routing/manifest/create.ts
+++ b/packages/astro/src/core/routing/manifest/create.ts
@@ -383,7 +383,8 @@ function createFileBasedRoutes(
 			} else {
 				components.push(item.file);
 				const component = item.file;
-				const { trailingSlash } = settings.config;
+				// Endpoints should have trailing slash
+				const trailingSlash = item.isPage ? settings.config.trailingSlash : 'never';
 				const pattern = getPattern(segments, settings.config, trailingSlash);
 				const generate = getRouteGenerator(segments, trailingSlash);
 				const pathname = segments.every((segment) => segment.length === 1 && !segment[0].dynamic)
diff --git a/packages/astro/test/astro-endpoint.test.js b/packages/astro/test/astro-endpoint.test.js
new file mode 100644
index 0000000000000..b3ef105dc22b7
--- /dev/null
+++ b/packages/astro/test/astro-endpoint.test.js
@@ -0,0 +1,23 @@
+import { before, it, after, describe } from 'node:test';
+import { loadFixture } from './test-utils.js';
+import assert from 'node:assert/strict';
+
+describe('Endpoint in dev, with trailing slash set to always', () => {
+	let fixture;
+	let devServer;
+
+	before(async () => {
+		fixture = await loadFixture({ root: './fixtures/astro-endpoint/' });
+		devServer = await fixture.startDevServer();
+	});
+
+	after(async () => {
+		await devServer.stop();
+	});
+
+	it('should render without issues', async () => {
+		let result = await fixture.fetch('/file.json');
+
+		assert.equal(result.status, 200);
+	});
+});
diff --git a/packages/astro/test/fixtures/astro-endpoint/astro.config.mjs b/packages/astro/test/fixtures/astro-endpoint/astro.config.mjs
new file mode 100644
index 0000000000000..8058fa63a39fd
--- /dev/null
+++ b/packages/astro/test/fixtures/astro-endpoint/astro.config.mjs
@@ -0,0 +1,6 @@
+import { defineConfig } from 'astro/config';
+
+// https://astro.build/config
+export default defineConfig({
+	trailingSlash: "always"
+});
diff --git a/packages/astro/test/fixtures/astro-endpoint/package.json b/packages/astro/test/fixtures/astro-endpoint/package.json
new file mode 100644
index 0000000000000..f57f66e1f6955
--- /dev/null
+++ b/packages/astro/test/fixtures/astro-endpoint/package.json
@@ -0,0 +1,8 @@
+{
+  "name": "@test/astro-endpoint",
+  "version": "0.0.0",
+  "private": true,
+  "dependencies": {
+    "astro": "workspace:*"
+  }
+}
diff --git a/packages/astro/test/fixtures/astro-endpoint/src/pages/file.json.js b/packages/astro/test/fixtures/astro-endpoint/src/pages/file.json.js
new file mode 100644
index 0000000000000..03f1de5cf3ddb
--- /dev/null
+++ b/packages/astro/test/fixtures/astro-endpoint/src/pages/file.json.js
@@ -0,0 +1 @@
+export const GET = () => Response.json({ success: true });
diff --git a/packages/astro/test/fixtures/astro-endpoint/src/pages/index.astro b/packages/astro/test/fixtures/astro-endpoint/src/pages/index.astro
new file mode 100644
index 0000000000000..e69de29bb2d1d
diff --git a/pnpm-lock.yaml b/pnpm-lock.yaml
index 1cd930ed3b79c..4ff3a2725bf2d 100644
--- a/pnpm-lock.yaml
+++ b/pnpm-lock.yaml
@@ -2006,6 +2006,12 @@ importers:
         specifier: ^4.2.5
         version: 4.2.8
 
+  packages/astro/test/fixtures/astro-endpoint:
+    dependencies:
+      astro:
+        specifier: workspace:*
+        version: link:../../..
+
   packages/astro/test/fixtures/astro-envs:
     dependencies:
       '@astrojs/vue':