diff --git a/.changeset/fuzzy-pots-worry.md b/.changeset/fuzzy-pots-worry.md
new file mode 100644
index 0000000000..f84531b502
--- /dev/null
+++ b/.changeset/fuzzy-pots-worry.md
@@ -0,0 +1,5 @@
+---
+'@backstage/plugin-kubernetes-backend': patch
+---
+
+K8s proxy HEADER_KUBERNETES_CLUSTER is now optional in single-cluster setups.
diff --git a/plugins/kubernetes-backend/src/service/KubernetesProxy.test.ts b/plugins/kubernetes-backend/src/service/KubernetesProxy.test.ts
index 4ed1c8a7ae..aaf3843e61 100644
--- a/plugins/kubernetes-backend/src/service/KubernetesProxy.test.ts
+++ b/plugins/kubernetes-backend/src/service/KubernetesProxy.test.ts
@@ -104,6 +104,56 @@ describe('KubernetesProxy', () => {
     ).rejects.toThrow(NotFoundError);
   });
 
+  it('should return a ERROR_NOT_FOUND if multi-cluster & no cluster selected', async () => {
+    clusterSupplier.getClusters.mockResolvedValue([
+      {
+        name: 'local',
+        url: 'http:/localhost:8001',
+        authProvider: 'localKubectlProxy',
+        skipMetricsLookup: true,
+      } as ClusterDetails,
+      {
+        name: 'cluster1',
+        url: 'https://localhost:9999',
+        serviceAccountToken: 'tokenA',
+        authProvider: 'googleServiceAccount',
+      } as ClusterDetails,
+    ]);
+
+    permissionApi.authorize.mockReturnValue(
+      Promise.resolve([{ result: AuthorizeResult.ALLOW }]),
+    );
+
+    const req = buildMockRequest(undefined, 'api');
+    const { res, next } = getMockRes();
+
+    await expect(
+      proxy.createRequestHandler({ permissionApi })(req, res, next),
+    ).rejects.toThrow(NotFoundError);
+  });
+
+  it('should return a ERROR_NOT_FOUND if selected cluster not in config', async () => {
+    clusterSupplier.getClusters.mockResolvedValue([
+      {
+        name: 'cluster1',
+        url: 'https://localhost:9999',
+        serviceAccountToken: 'tokenA',
+        authProvider: 'googleServiceAccount',
+      } as ClusterDetails,
+    ]);
+
+    permissionApi.authorize.mockReturnValue(
+      Promise.resolve([{ result: AuthorizeResult.ALLOW }]),
+    );
+
+    const req = buildMockRequest('test', 'api');
+    const { res, next } = getMockRes();
+
+    await expect(
+      proxy.createRequestHandler({ permissionApi })(req, res, next),
+    ).rejects.toThrow(NotFoundError);
+  });
+
   it('should pass the exact response from Kubernetes', async () => {
     const apiResponse = {
       kind: 'APIVersions',
@@ -155,6 +205,55 @@ describe('KubernetesProxy', () => {
     expect(response.body).toStrictEqual(apiResponse);
   });
 
+  it('should pass the exact response from Kubernetes default cluster & no cluster selected in single cluster setup', async () => {
+    const apiResponse = {
+      kind: 'APIVersions',
+      versions: ['v1'],
+      serverAddressByClientCIDRs: [
+        {
+          clientCIDR: '0.0.0.0/0',
+          serverAddress: '192.168.0.1:3333',
+        },
+      ],
+    };
+
+    clusterSupplier.getClusters.mockResolvedValue([
+      {
+        name: 'cluster1',
+        url: 'https://localhost:9999',
+        serviceAccountToken: '',
+        authProvider: 'serviceAccount',
+      },
+    ] as ClusterDetails[]);
+
+    permissionApi.authorize.mockReturnValue(
+      Promise.resolve([{ result: AuthorizeResult.ALLOW }]),
+    );
+
+    authTranslator.decorateClusterDetailsWithAuth.mockResolvedValue({
+      name: 'cluster1',
+      url: 'https://localhost:9999',
+      serviceAccountToken: '',
+      authProvider: 'serviceAccount',
+    } as ClusterDetails);
+
+    const router = Router();
+    router.use('/mountpath', proxy.createRequestHandler({ permissionApi }));
+    const app = express().use(router);
+    const requestPromise = request(app).get('/mountpath/api');
+    worker.use(
+      rest.get('https://localhost:9999/api', (_: any, res: any, ctx: any) =>
+        res(ctx.status(299), ctx.json(apiResponse)),
+      ),
+      rest.all(requestPromise.url, (req: any) => req.passthrough()),
+    );
+
+    const response = await requestPromise;
+
+    expect(response.status).toEqual(299);
+    expect(response.body).toStrictEqual(apiResponse);
+  });
+
   it('sets host header to support clusters behind name-based virtual hosts', async () => {
     worker.use(
       rest.get(
@@ -481,55 +580,6 @@ describe('KubernetesProxy', () => {
     });
   });
 
-  it('should return a 400 error if Backstage-Kubernetes-Cluster field isnt provided in request', async () => {
-    worker.use(
-      rest.get('https://localhost:9999/api/v1/namespaces', (_req, res, ctx) => {
-        return res(
-          ctx.status(200),
-          ctx.json({
-            kind: 'NamespaceList',
-            apiVersion: 'v1',
-            items: [],
-          }),
-        );
-      }),
-    );
-
-    permissionApi.authorize.mockReturnValue(
-      Promise.resolve([{ result: AuthorizeResult.ALLOW }]),
-    );
-
-    clusterSupplier.getClusters.mockResolvedValue([
-      {
-        name: 'cluster1',
-        url: 'https://localhost:9999',
-        authProvider: 'googleServiceAccount',
-      },
-    ] as ClusterDetails[]);
-
-    authTranslator.decorateClusterDetailsWithAuth.mockResolvedValue({
-      name: 'cluster1',
-      url: 'https://localhost:9999',
-      serviceAccountToken: 'tokenA',
-      authProvider: 'googleServiceAccount',
-    } as ClusterDetails);
-
-    const router = Router();
-    router.use('/mountpath', proxy.createRequestHandler({ permissionApi }));
-    router.use(errorHandler());
-    const app = express().use(router);
-
-    const requestPromise = request(app)
-      .get('/mountpath/api/v1/namespaces')
-      .set(HEADER_KUBERNETES_AUTH, 'tokenB');
-
-    worker.use(rest.all(requestPromise.url, (req: any) => req.passthrough()));
-
-    const response = await requestPromise;
-
-    expect(response.status).toEqual(400);
-  });
-
   it('returns a 500 error if authTranslator errors out and Backstage-Kubernetes-Authorization field is not provided', async () => {
     worker.use(
       rest.get('https://localhost:9999/api/v1/namespaces', (req, res, ctx) => {
diff --git a/plugins/kubernetes-backend/src/service/KubernetesProxy.ts b/plugins/kubernetes-backend/src/service/KubernetesProxy.ts
index b4ca87d6f0..8e8fd54c77 100644
--- a/plugins/kubernetes-backend/src/service/KubernetesProxy.ts
+++ b/plugins/kubernetes-backend/src/service/KubernetesProxy.ts
@@ -17,7 +17,6 @@
 import {
   ErrorResponseBody,
   ForwardedError,
-  InputError,
   NotAllowedError,
   NotFoundError,
   serializeError,
@@ -175,13 +174,23 @@ export class KubernetesProxy {
 
   private async getClusterForRequest(req: Request): Promise<ClusterDetails> {
     const clusterName = req.header(HEADER_KUBERNETES_CLUSTER);
-    if (!clusterName) {
-      throw new InputError(`Missing '${HEADER_KUBERNETES_CLUSTER}' header.`);
+    const clusters = await this.clusterSupplier.getClusters();
+
+    if (!clusters || clusters.length <= 0) {
+      throw new NotFoundError(`No Clusters configured`);
+    }
+
+    const hasClusterNameHeader =
+      typeof clusterName === 'string' && clusterName.length > 0;
+
+    let cluster: ClusterDetails | undefined;
+
+    if (hasClusterNameHeader) {
+      cluster = clusters.find(c => c.name === clusterName);
+    } else if (clusters.length === 1) {
+      cluster = clusters.at(0);
     }
 
-    const cluster = await this.clusterSupplier
-      .getClusters()
-      .then(clusters => clusters.find(c => c.name === clusterName));
     if (!cluster) {
       throw new NotFoundError(`Cluster '${clusterName}' not found`);
     }