diff --git a/src/backend/server.test.ts b/src/backend/server.test.ts
index f3d9fd5f5..17ab78c26 100644
--- a/src/backend/server.test.ts
+++ b/src/backend/server.test.ts
@@ -468,6 +468,58 @@ describe('PuterServer host header validation — permissive modes', () => {
     });
 });
 
+describe('PuterServer host header validation — custom domains with every host accepted', () => {
+    let server: PuterServer;
+    let port: number;
+
+    beforeAll(async () => {
+        port = await allocateEphemeralPort();
+        server = await setupTestServer(
+            {
+                port,
+                domain: 'puter.localhost',
+                origin: `http://puter.localhost:${port}`,
+                allow_all_host_values: true,
+                custom_domains_enabled: true,
+                static_hosting_domain: 'site.puter.localhost',
+            } as unknown as IConfig,
+            { listen: true },
+        );
+    });
+
+    afterAll(async () => {
+        await server?.shutdown();
+    });
+
+    it('still hands a host outside our domains to site hosting', async () => {
+        const res = await rawRequest(port, '/', {
+            host: 'www.my-own-domain.example',
+        });
+        expect(res.status).toBe(404);
+        expect(res.body).toBe('Site not found');
+    });
+
+    it('leaves our own domain to the GUI', async () => {
+        const res = await rawRequest(port, '/healthcheck', {
+            host: `puter.localhost:${port}`,
+        });
+        expect(res.status).toBe(200);
+    });
+
+    it('never treats an IP or localhost as a custom domain', async () => {
+        for (const host of [
+            `127.0.0.1:${port}`,
+            `[::1]:${port}`,
+            `localhost:${port}`,
+        ]) {
+            const res = await rawRequest(port, '/healthcheck', { host });
+            expect(res.status, host).toBe(200);
+            const root = await rawRequest(port, '/', { host });
+            expect(root.body, host).not.toBe('Site not found');
+        }
+    });
+});
+
 describe('PuterServer request parsing', () => {
     let server: PuterServer;
     let port: number;
diff --git a/src/backend/server.ts b/src/backend/server.ts
index 927b04919..c87aee715 100644
--- a/src/backend/server.ts
+++ b/src/backend/server.ts
@@ -29,6 +29,7 @@ import path from 'node:path';
 import { pathToFileURL } from 'node:url';
 import { parseArgs } from 'node:util';
 import http from 'node:http';
+import { isIP } from 'node:net';
 import { puterClients } from './clients';
 import { puterControllers } from './controllers';
 import { createAuthProbe } from './core/http/middleware/authProbe';
@@ -597,7 +598,32 @@ export class PuterServer {
 
         // Build the allowed-domain set from config.
         this.#app.use((req, res, next) => {
+            const hostName = (req.headers.host ?? '')
+                .split(':')[0]
+                .trim()
+                .toLowerCase();
+            const isOwnHost =
+                !hostName ||
+                this.#getAllowedDomains().some((d) =>
+                    PuterServer.#hostMatchesDomain(hostName, d),
+                );
+
+            // Accepting every host still has to tell custom domains apart, or
+            // they fall through to the API/GUI instead of site hosting. An IP
+            // or localhost is never one: load balancer health checks and
+            // in-cluster callers address the server that way.
             if (config.allow_all_host_values) {
+                if (
+                    config.custom_domains_enabled &&
+                    !isOwnHost &&
+                    req.path !== '/healthcheck' &&
+                    // `[` is what an IPv6 literal's `[::1]:port` splits to.
+                    !hostName.startsWith('[') &&
+                    isIP(hostName) === 0 &&
+                    hostName !== 'localhost'
+                ) {
+                    req.is_custom_domain = true;
+                }
                 next();
                 return;
             }
@@ -613,15 +639,7 @@ export class PuterServer {
                 return;
             }
 
-            const hostName = (req.headers.host ?? '')
-                .split(':')[0]
-                .trim()
-                .toLowerCase();
-            const allowed = this.#getAllowedDomains();
-
-            if (
-                allowed.some((d) => PuterServer.#hostMatchesDomain(hostName, d))
-            ) {
+            if (isOwnHost) {
                 next();
                 return;
             }