diff --git a/docs/errors/no_new_actions_at_runtime.md b/docs/errors/no_new_actions_at_runtime.md
new file mode 100644
index 0000000000..cfed39eac7
--- /dev/null
+++ b/docs/errors/no_new_actions_at_runtime.md
@@ -0,0 +1,22 @@
+# No new actions at runtime error
+
+Defining new actions at runtime is not allowed.
+
+✅ DO:
+
+```ts
+const prompt = defineDotprompt({...})
+
+const flow = defineFlow({...}, async (input) => {
+  await prompt.generate(...);
+})
+```
+
+❌ DON'T:
+
+```ts
+const flow = defineFlow({...}, async (input) => {
+  const prompt = defineDotprompt({...})
+  prompt.generate(...);
+})
+```
diff --git a/js/core/src/action.ts b/js/core/src/action.ts
index a78c8a724f..182995b8fd 100644
--- a/js/core/src/action.ts
+++ b/js/core/src/action.ts
@@ -18,7 +18,12 @@ import { JSONSchema7 } from 'json-schema';
 import { AsyncLocalStorage } from 'node:async_hooks';
 import { performance } from 'node:perf_hooks';
 import * as z from 'zod';
-import { ActionType, lookupPlugin, registerAction } from './registry.js';
+import {
+  ActionType,
+  initializeAllPlugins,
+  lookupPlugin,
+  registerAction,
+} from './registry.js';
 import { parseSchema } from './schema.js';
 import * as telemetry from './telemetry.js';
 import {
@@ -216,9 +221,16 @@ export function defineAction<
   },
   fn: (input: z.infer<I>) => Promise<z.infer<O>>
 ): Action<I, O> {
-  const act = action(config, (i: I): Promise<z.infer<O>> => {
+  if (isInRuntimeContext()) {
+    throw new Error(
+      'Cannot define new actions at runtime.\n' +
+        'See: https://github.com/firebase/genkit/blob/main/docs/errors/no_new_actions_at_runtime.md'
+    );
+  }
+  const act = action(config, async (i: I): Promise<z.infer<O>> => {
     setCustomMetadataAttributes({ subtype: config.actionType });
-    return fn(i);
+    await initializeAllPlugins();
+    return await runInActionRuntimeContext(() => fn(i));
   });
   act.__action.actionType = config.actionType;
   registerAction(config.actionType, act);
@@ -252,3 +264,19 @@ export function getStreamingCallback<S>(): StreamingCallback<S> | undefined {
   }
   return cb;
 }
+
+const runtimeCtxAls = new AsyncLocalStorage<any>();
+
+/**
+ * Checks whether the caller is currently in the runtime context of an action.
+ */
+export function isInRuntimeContext() {
+  return !!runtimeCtxAls.getStore();
+}
+
+/**
+ * Execute the provided function in the action runtime context.
+ */
+export function runInActionRuntimeContext<R>(fn: () => R) {
+  return runtimeCtxAls.run('runtime', fn);
+}
diff --git a/js/core/src/plugin.ts b/js/core/src/plugin.ts
index a21a3a5f3d..97955ce002 100644
--- a/js/core/src/plugin.ts
+++ b/js/core/src/plugin.ts
@@ -15,7 +15,7 @@
  */
 
 import { z } from 'zod';
-import { Action } from './action.js';
+import { Action, isInRuntimeContext } from './action.js';
 import { FlowStateStore } from './flowTypes.js';
 import { LoggerConfig, TelemetryConfig } from './telemetryTypes.js';
 import { TraceStore } from './tracing.js';
@@ -60,6 +60,12 @@ export function genkitPlugin<T extends PluginInit>(
   pluginName: string,
   initFn: T
 ): Plugin<Parameters<T>> {
+  if (isInRuntimeContext()) {
+    throw new Error(
+      'Cannot define new plugins at runtime.\n' +
+        'See: https://github.com/firebase/genkit/blob/main/docs/errors/no_new_actions_at_runtime.md'
+    );
+  }
   return (...args: Parameters<T>) => ({
     name: pluginName,
     initializer: async () => {
diff --git a/js/core/src/registry.ts b/js/core/src/registry.ts
index 94647c92be..b46b636baf 100644
--- a/js/core/src/registry.ts
+++ b/js/core/src/registry.ts
@@ -126,10 +126,19 @@ type ActionsRecord = Record<string, Action<z.ZodTypeAny, z.ZodTypeAny>>;
  * Returns all actions in the registry.
  */
 export async function listActions(): Promise<ActionsRecord> {
+  await initializeAllPlugins();
+  return Object.assign({}, actionsById());
+}
+
+let allPluginsInitialized = false;
+export async function initializeAllPlugins() {
+  if (allPluginsInitialized) {
+    return;
+  }
   for (const pluginName of Object.keys(pluginsByName())) {
     await initializePlugin(pluginName);
   }
-  return Object.assign({}, actionsById());
+  allPluginsInitialized = true;
 }
 
 /**
@@ -195,14 +204,17 @@ export async function lookupFlowStateStore(
  * Registers a flow state store for the given environment.
  */
 export function registerPluginProvider(name: string, provider: PluginProvider) {
+  allPluginsInitialized = false;
   let cached;
+  let isInitialized = false;
   pluginsByName()[name] = {
     name: provider.name,
     initializer: () => {
-      if (cached) {
+      if (isInitialized) {
         return cached;
       }
       cached = provider.initializer();
+      isInitialized = true;
       return cached;
     },
   };
diff --git a/js/flow/src/flow.ts b/js/flow/src/flow.ts
index 8d318a1c33..1eb51fb7b3 100644
--- a/js/flow/src/flow.ts
+++ b/js/flow/src/flow.ts
@@ -28,6 +28,7 @@ import {
   StreamingCallback,
 } from '@genkit-ai/core';
 import { logger } from '@genkit-ai/core/logging';
+import { initializeAllPlugins } from '@genkit-ai/core/registry';
 import { toJsonSchema } from '@genkit-ai/core/schema';
 import {
   newTrace,
@@ -391,6 +392,7 @@ export class Flow<
     labels: Record<string, string> | undefined
   ) {
     const startTimeMs = performance.now();
+    await initializeAllPlugins();
     await runWithActiveContext(ctx, async () => {
       let traceContext;
       if (ctx.state.traceContext) {
diff --git a/js/flow/src/utils.ts b/js/flow/src/utils.ts
index 774d81c4cd..4110195175 100644
--- a/js/flow/src/utils.ts
+++ b/js/flow/src/utils.ts
@@ -14,6 +14,7 @@
  * limitations under the License.
  */
 
+import { runInActionRuntimeContext } from '@genkit-ai/core';
 import { AsyncLocalStorage } from 'node:async_hooks';
 import { v4 as uuidv4 } from 'uuid';
 import z from 'zod';
@@ -45,7 +46,7 @@ export function runWithActiveContext<R>(
   ctx: Context<z.ZodTypeAny, z.ZodTypeAny, z.ZodTypeAny>,
   fn: () => R
 ) {
-  return ctxAsyncLocalStorage.run(ctx, fn);
+  return ctxAsyncLocalStorage.run(ctx, () => runInActionRuntimeContext(fn));
 }
 
 /**