diff --git a/js/ai/src/generate.ts b/js/ai/src/generate.ts
index d5c0abf168..c84f47b13e 100755
--- a/js/ai/src/generate.ts
+++ b/js/ai/src/generate.ts
@@ -190,6 +190,13 @@ export async function toGenerateRequest(
   registry: Registry,
   options: GenerateOptions
 ): Promise<GenerateRequest> {
+  if (options.prompt && options.resume) {
+    throw new GenkitError({
+      status: 'INVALID_ARGUMENT',
+      message:
+        'prompt is not supported when resume is set. The message history in messages is used instead.',
+    });
+  }
   const messages: MessageData[] = [];
   if (options.system) {
     messages.push({
@@ -200,7 +207,7 @@ export async function toGenerateRequest(
   if (options.messages) {
     messages.push(...options.messages.map((m) => Message.parseData(m)));
   }
-  if (options.prompt) {
+  if (options.prompt && !options.resume) {
     messages.push({
       role: 'user',
       content: Message.parseContent(options.prompt),
@@ -333,6 +340,13 @@ async function resourcesToActionRefs(
 }
 
 function messagesFromOptions(options: GenerateOptions): MessageData[] {
+  if (options.prompt && options.resume) {
+    throw new GenkitError({
+      status: 'INVALID_ARGUMENT',
+      message:
+        'prompt is not supported when resume is set. The message history in messages is used instead.',
+    });
+  }
   const messages: MessageData[] = [];
   if (options.system) {
     messages.push({
@@ -343,7 +357,7 @@ function messagesFromOptions(options: GenerateOptions): MessageData[] {
   if (options.messages) {
     messages.push(...options.messages);
   }
-  if (options.prompt) {
+  if (options.prompt && !options.resume) {
     messages.push({
       role: 'user',
       content: Message.parseContent(options.prompt),
diff --git a/js/ai/src/prompt.ts b/js/ai/src/prompt.ts
index 1c489ad189..a4dd2a6cae 100644
--- a/js/ai/src/prompt.ts
+++ b/js/ai/src/prompt.ts
@@ -629,6 +629,7 @@ async function renderUserPrompt<
   promptCache: PromptCache,
   renderOptions: PromptGenerateOptions<O, CustomOptions> | undefined
 ) {
+  if (renderOptions?.resume) return;
   if (typeof options.prompt === 'function') {
     messages.push({
       role: 'user',
diff --git a/js/ai/tests/generate/generate_test.ts b/js/ai/tests/generate/generate_test.ts
index a45c3ab0e8..c428a40538 100644
--- a/js/ai/tests/generate/generate_test.ts
+++ b/js/ai/tests/generate/generate_test.ts
@@ -296,6 +296,28 @@ describe('toGenerateRequest', () => {
       },
       throws: 'FAILED_PRECONDITION',
     },
+    {
+      should: 'throw INVALID_ARGUMENT when both prompt and resume are set',
+      prompt: {
+        messages: [
+          { role: 'user', content: [{ text: 'hi' }] },
+          {
+            role: 'model',
+            content: [
+              { text: 'there' },
+              { toolRequest: { name: 'test', input: { x: 1 } } },
+            ],
+          },
+        ],
+        prompt: 'count to 10',
+        resume: {
+          respond: {
+            toolResponse: { name: 'test', output: { done: true } },
+          },
+        },
+      },
+      throws: 'INVALID_ARGUMENT',
+    },
     {
       should: 'passes through output options',
       prompt: {