diff --git a/js/ai/src/prompt.ts b/js/ai/src/prompt.ts
index aa228bd084..4d9ee77c5c 100644
--- a/js/ai/src/prompt.ts
+++ b/js/ai/src/prompt.ts
@@ -875,7 +875,7 @@ export async function prompt<
 >(
   registry: Registry,
   name: string,
-  options?: { variant?: string; dir?: string }
+  options?: { variant?: string; dir?: string | null }
 ): Promise<ExecutablePrompt<I, O, CustomOptions>> {
   return await lookupPrompt<I, O, CustomOptions>(
     registry,
diff --git a/js/genkit/src/genkit.ts b/js/genkit/src/genkit.ts
index 01333ae7d9..92ba1d4724 100644
--- a/js/genkit/src/genkit.ts
+++ b/js/genkit/src/genkit.ts
@@ -160,8 +160,8 @@ export type PromptFn<
 export interface GenkitOptions {
   /** List of plugins to load. */
   plugins?: (GenkitPlugin | GenkitPluginV2)[];
-  /** Directory where dotprompts are stored. */
-  promptDir?: string;
+  /** Directory where dotprompts are stored. Set to `null` to disable automatic prompt loading. */
+  promptDir?: string | null;
   /** Default model to use if no model is specified. */
   model?: ModelArgument<any>;
   /** Additional runtime context data for flows and tools. */
@@ -360,7 +360,10 @@ export class Genkit implements HasRegistry {
       `${name}${options?.variant ? `.${options?.variant}` : ''}`,
       prompt(this.registry, name, {
         ...options,
-        dir: this.options.promptDir ?? './prompts',
+        dir:
+          this.options.promptDir === undefined
+            ? './prompts'
+            : this.options.promptDir,
       })
     );
   }
diff --git a/js/genkit/tests/prompts_test.ts b/js/genkit/tests/prompts_test.ts
index 7db00cd165..9f6e429a91 100644
--- a/js/genkit/tests/prompts_test.ts
+++ b/js/genkit/tests/prompts_test.ts
@@ -1057,6 +1057,19 @@ describe('prompt', () => {
     });
   });
 
+  it('does not auto-load prompts when promptDir is null', async () => {
+    const aiWithoutPromptDir = genkit({
+      model: 'echoModel',
+      promptDir: null,
+    });
+
+    const prompt = aiWithoutPromptDir.prompt('test');
+    const response = prompt();
+    await assert.rejects(response, {
+      message: 'NOT_FOUND: Prompt test not found',
+    });
+  });
+
   it('loads from from the sub folder', async () => {
     const testPrompt = ai.prompt('sub/test'); // see tests/prompts/sub folder