diff --git a/packages/@aws-cdk/aws-amplify-alpha/lib/app.ts b/packages/@aws-cdk/aws-amplify-alpha/lib/app.ts
index 057d413961dbd..ffcc482811ba6 100644
--- a/packages/@aws-cdk/aws-amplify-alpha/lib/app.ts
+++ b/packages/@aws-cdk/aws-amplify-alpha/lib/app.ts
@@ -316,7 +316,9 @@ export class App extends Resource implements IApp, iam.IGrantable {
       name: props.appName || this.node.id,
       oauthToken: sourceCodeProviderOptions?.oauthToken?.unsafeUnwrap(), // Safe usage
       repository: sourceCodeProviderOptions?.repository,
-      customHeaders: props.customResponseHeaders ? renderCustomResponseHeaders(props.customResponseHeaders, this) : undefined,
+      customHeaders: props.customResponseHeaders && props.customResponseHeaders.length > 0
+        ? renderCustomResponseHeaders(props.customResponseHeaders, this)
+        : undefined,
       platform: appPlatform,
       jobConfig: props.buildComputeType ? { buildComputeType: props.buildComputeType } : undefined,
     });
@@ -594,7 +596,21 @@ export interface CustomResponseHeader {
   readonly headers: { [key: string]: string };
 }
 
+/**
+ * Renders custom response headers to YAML format.
+ *
+ * @param customHeaders - Array of custom headers. Must not be empty.
+ * @param scope - Construct scope for error reporting
+ * @returns YAML string representation of custom headers
+ *
+ * @internal
+ */
 function renderCustomResponseHeaders(customHeaders: CustomResponseHeader[], scope: IConstruct): string {
+  // Defensive assertion - should never happen due to call site validation
+  if (customHeaders.length === 0) {
+    throw new ValidationError('renderCustomResponseHeaders called with empty array', scope);
+  }
+
   const hasAppRoot = customHeaders[0].appRoot !== undefined;
   const yaml = [hasAppRoot ? 'applications:' : 'customHeaders:'];
 
diff --git a/packages/@aws-cdk/aws-amplify-alpha/test/app.test.ts b/packages/@aws-cdk/aws-amplify-alpha/test/app.test.ts
index 6903d23d7ff27..0a2814a7ec0e1 100644
--- a/packages/@aws-cdk/aws-amplify-alpha/test/app.test.ts
+++ b/packages/@aws-cdk/aws-amplify-alpha/test/app.test.ts
@@ -1,4 +1,4 @@
-import { Template } from 'aws-cdk-lib/assertions';
+import { Template, Match } from 'aws-cdk-lib/assertions';
 import * as codebuild from 'aws-cdk-lib/aws-codebuild';
 import * as codecommit from 'aws-cdk-lib/aws-codecommit';
 import * as iam from 'aws-cdk-lib/aws-iam';
@@ -549,6 +549,24 @@ test('error with inconsistent appRoot in custom headers', () => {
   }).toThrow('appRoot must be either be present or absent across all custom response headers');
 });
 
+test('with empty custom response headers array', () => {
+  // WHEN - Empty array should be handled gracefully (regression test for #35693)
+  new amplify.App(stack, 'App', {
+    sourceCodeProvider: new amplify.GitHubSourceCodeProvider({
+      owner: 'aws',
+      repository: 'aws-cdk',
+      oauthToken: SecretValue.unsafePlainText('secret'),
+    }),
+    customResponseHeaders: [],
+  });
+
+  // THEN - CustomHeaders property should be omitted from CloudFormation
+  Template.fromStack(stack).hasResourceProperties('AWS::Amplify::App', {
+    Name: 'App',
+    CustomHeaders: Match.absent(),
+  });
+});
+
 test('create a statically hosted app by default', () => {
   // WHEN
   new amplify.App(stack, 'App', {});