diff --git a/ee/lib/ee/api/internal/kubernetes.rb b/ee/lib/ee/api/internal/kubernetes.rb
index d4481f325aa5032adcde60eebdd1be7c61ed107d..08bc8919105d8817aa8069c602f1d2f6afeb711b 100644
--- a/ee/lib/ee/api/internal/kubernetes.rb
+++ b/ee/lib/ee/api/internal/kubernetes.rb
@@ -83,6 +83,14 @@ def update_configuration(agent:, config:)
                     forbidden!('"remote_development" licensed feature is not available')
                   end
 
+                  unless agent.unversioned_latest_workspaces_agent_config
+                    render_api_error!(
+                      'The remote development workspaces config for the agent is invalid. ' \
+                        'Please see https://docs.gitlab.com/user/workspace/settings/#configuration-reference',
+                      406
+                    )
+                  end
+
                   domain_main_class_args = {
                     agent: agent
                   }
diff --git a/ee/spec/requests/api/internal/kubernetes_spec.rb b/ee/spec/requests/api/internal/kubernetes_spec.rb
index 5905e8b9a3dd18caa69dfaefca39ca82744b3eb1..6bac5ac7de937c5112d5d842e3062337238acb21 100644
--- a/ee/spec/requests/api/internal/kubernetes_spec.rb
+++ b/ee/spec/requests/api/internal/kubernetes_spec.rb
@@ -145,6 +145,9 @@ def send_request(params: {}, headers: agent_token_headers)
 
     before do
       stub_licensed_features(remote_development: true)
+      # rubocop:disable RSpec/AnyInstanceOf -- It's NOT the next instance...
+      allow_any_instance_of(Clusters::Agent).to receive(:unversioned_latest_workspaces_agent_config).and_return(true)
+      # rubocop:enable RSpec/AnyInstanceOf
     end
 
     include_examples 'authorization'
@@ -179,6 +182,22 @@ def send_request(params: {}, headers: agent_token_headers)
       end
     end
 
+    context 'when agent config not found' do
+      before do
+        # rubocop:disable RSpec/AnyInstanceOf -- It's NOT the next instance...
+        allow_any_instance_of(Clusters::Agent).to receive(:unversioned_latest_workspaces_agent_config).and_return(nil)
+        # rubocop:enable RSpec/AnyInstanceOf
+      end
+
+      it 'returns service response with error 406' do
+        expect(RemoteDevelopment::CommonService).not_to receive(:execute)
+
+        send_request
+
+        expect(response).to have_gitlab_http_status(:not_acceptable)
+      end
+    end
+
     context 'when remote_development feature is unlicensed' do
       before do
         stub_licensed_features(remote_development: false)