diff --git a/packages/examples/packages/lifecycle-hooks/README.md b/packages/examples/packages/lifecycle-hooks/README.md
index a740b83472..58e1631705 100644
--- a/packages/examples/packages/lifecycle-hooks/README.md
+++ b/packages/examples/packages/lifecycle-hooks/README.md
@@ -1,7 +1,7 @@
 # `@metamask/lifecylce-hooks-example-snap`
 
-This snap demonstrates how to use the `onInstall` and `onUpdate` lifecycle
-hooks.
+This Snap demonstrates how to use the `onStart`, `onInstall`, and `onUpdate`
+lifecycle hooks.
 
 ## Snap manifest
 
@@ -22,9 +22,9 @@ Along with other permissions, the manifest of this snap includes the
 
 ## Snap usage
 
-This snap exposes the `onInstall` and `onUpdate` lifecycle hooks. These hooks
-are called when the snap is installed or updated, respectively, and cannot be
-called manually.
+This Snap exposes the `onStart`, `onInstall`, and `onUpdate` lifecycle hooks.
+These hooks are called when the client is started, when the Snap is installed,
+or the Snap is updated, respectively, and cannot be called manually.
 
 For more information, you can refer to
 [the end-to-end tests](./src/index.test.ts).
diff --git a/packages/examples/packages/lifecycle-hooks/package.json b/packages/examples/packages/lifecycle-hooks/package.json
index fd12cf32bc..ca5e47f023 100644
--- a/packages/examples/packages/lifecycle-hooks/package.json
+++ b/packages/examples/packages/lifecycle-hooks/package.json
@@ -1,7 +1,7 @@
 {
   "name": "@metamask/lifecycle-hooks-example-snap",
   "version": "2.1.3",
-  "description": "MetaMask example snap demonstrating the use of the `onInstall` and `onUpdate` lifecycle hooks",
+  "description": "MetaMask example snap demonstrating the use of the `onStart`, `onInstall`, and `onUpdate` lifecycle hooks",
   "keywords": [
     "MetaMask",
     "Snaps",
diff --git a/packages/examples/packages/lifecycle-hooks/snap.manifest.json b/packages/examples/packages/lifecycle-hooks/snap.manifest.json
index 64db943321..6183e6b835 100644
--- a/packages/examples/packages/lifecycle-hooks/snap.manifest.json
+++ b/packages/examples/packages/lifecycle-hooks/snap.manifest.json
@@ -1,13 +1,13 @@
 {
   "version": "2.1.3",
-  "description": "MetaMask example snap demonstrating the use of the `onInstall` and `onUpdate` lifecycle hooks.",
+  "description": "MetaMask example snap demonstrating the use of the `onStart`, `onInstall`, and `onUpdate` lifecycle hooks.",
   "proposedName": "Lifecycle Hooks Example Snap",
   "repository": {
     "type": "git",
     "url": "https://github.com/MetaMask/snaps.git"
   },
   "source": {
-    "shasum": "q+mPr3Gq/2PZDIrqKu+wR7sh1hwKk+F5OoEo1ye+30Q=",
+    "shasum": "c6HavArVNGdBQlFYdVeKXpahvU0DHpB6D6UupoexRR0=",
     "location": {
       "npm": {
         "filePath": "dist/bundle.js",
diff --git a/packages/examples/packages/lifecycle-hooks/src/index.test.tsx b/packages/examples/packages/lifecycle-hooks/src/index.test.tsx
index 47433b59ab..639a3c0460 100644
--- a/packages/examples/packages/lifecycle-hooks/src/index.test.tsx
+++ b/packages/examples/packages/lifecycle-hooks/src/index.test.tsx
@@ -2,6 +2,30 @@ import { describe, expect, it } from '@jest/globals';
 import { assertIsAlertDialog, installSnap } from '@metamask/snaps-jest';
 import { Box, Text } from '@metamask/snaps-sdk/jsx';
 
+describe('onStart', () => {
+  it('shows dialog when the client is started', async () => {
+    const { onStart } = await installSnap();
+
+    const response = onStart();
+
+    const screen = await response.getInterface();
+    assertIsAlertDialog(screen);
+
+    expect(screen).toRender(
+      <Box>
+        <Text>
+          The client was started successfully, and the "onStart" handler was
+          called.
+        </Text>
+      </Box>,
+    );
+
+    await screen.ok();
+
+    expect(await response).toRespondWith(null);
+  });
+});
+
 describe('onInstall', () => {
   it('shows dialog when the snap is installed', async () => {
     const { onInstall } = await installSnap();
diff --git a/packages/examples/packages/lifecycle-hooks/src/index.tsx b/packages/examples/packages/lifecycle-hooks/src/index.tsx
index b429cc701a..2051992a03 100644
--- a/packages/examples/packages/lifecycle-hooks/src/index.tsx
+++ b/packages/examples/packages/lifecycle-hooks/src/index.tsx
@@ -1,6 +1,37 @@
-import type { OnInstallHandler, OnUpdateHandler } from '@metamask/snaps-sdk';
+import type {
+  OnInstallHandler,
+  OnStartHandler,
+  OnUpdateHandler,
+} from '@metamask/snaps-sdk';
 import { Box, Text } from '@metamask/snaps-sdk/jsx';
 
+/**
+ * Handle starting of the client. This handler is called when the client is
+ * started, and can be used to perform any initialization that is required.
+ *
+ * This handler is optional. If it is not provided, the Snap will be started
+ * as usual.
+ *
+ * @see https://docs.metamask.io/snaps/reference/entry-points/#onstart
+ * @returns The JSON-RPC response.
+ */
+export const onStart: OnStartHandler = async () => {
+  return await snap.request({
+    method: 'snap_dialog',
+    params: {
+      type: 'alert',
+      content: (
+        <Box>
+          <Text>
+            The client was started successfully, and the "onStart" handler was
+            called.
+          </Text>
+        </Box>
+      ),
+    },
+  });
+};
+
 /**
  * Handle installation of the snap. This handler is called when the snap is
  * installed, and can be used to perform any initialization that is required.'
@@ -8,7 +39,7 @@ import { Box, Text } from '@metamask/snaps-sdk/jsx';
  * This handler is optional. If it is not provided, the snap will be installed
  * as usual.
  *
- * @see https://docs.metamask.io/snaps/reference/exports/#oninstall
+ * @see https://docs.metamask.io/snaps/reference/entry-points/#oninstall
  * @returns The JSON-RPC response.
  */
 export const onInstall: OnInstallHandler = async () => {
@@ -35,7 +66,7 @@ export const onInstall: OnInstallHandler = async () => {
  * This handler is optional. If it is not provided, the snap will be updated
  * as usual.
  *
- * @see https://docs.metamask.io/snaps/reference/exports/#onupdate
+ * @see https://docs.metamask.io/snaps/reference/entry-points/#onupdate
  * @returns The JSON-RPC response.
  */
 export const onUpdate: OnUpdateHandler = async () => {
diff --git a/packages/snaps-controllers/coverage.json b/packages/snaps-controllers/coverage.json
index 287f895bda..6d89f22e62 100644
--- a/packages/snaps-controllers/coverage.json
+++ b/packages/snaps-controllers/coverage.json
@@ -1,6 +1,6 @@
 {
-  "branches": 95.21,
-  "functions": 98.71,
+  "branches": 95.22,
+  "functions": 98.72,
   "lines": 98.87,
-  "statements": 98.7
+  "statements": 98.71
 }
diff --git a/packages/snaps-controllers/src/snaps/SnapController.test.tsx b/packages/snaps-controllers/src/snaps/SnapController.test.tsx
index 9d13b59bef..2a031d830d 100644
--- a/packages/snaps-controllers/src/snaps/SnapController.test.tsx
+++ b/packages/snaps-controllers/src/snaps/SnapController.test.tsx
@@ -9889,6 +9889,127 @@ describe('SnapController', () => {
   });
 
   describe('SnapController actions', () => {
+    describe('SnapController:init', () => {
+      it('calls `onStart` for all Snaps with the `endowment:lifecycle-hooks` permission', async () => {
+        const rootMessenger = getControllerMessenger();
+        const messenger = getSnapControllerMessenger(rootMessenger);
+
+        rootMessenger.registerActionHandler(
+          'PermissionController:getPermissions',
+          (origin) => {
+            if (origin === MOCK_SNAP_ID) {
+              return {
+                [SnapEndowments.LifecycleHooks]:
+                  MOCK_LIFECYCLE_HOOKS_PERMISSION,
+              };
+            }
+
+            return {};
+          },
+        );
+
+        rootMessenger.registerActionHandler(
+          'PermissionController:hasPermission',
+          (origin) => {
+            return origin === MOCK_SNAP_ID;
+          },
+        );
+
+        const snapController = getSnapController(
+          getSnapControllerOptions({
+            messenger,
+            state: {
+              snaps: getPersistedSnapsState(
+                getPersistedSnapObject({
+                  id: MOCK_SNAP_ID,
+                }),
+                getPersistedSnapObject({
+                  id: MOCK_LOCAL_SNAP_ID,
+                }),
+              ),
+            },
+          }),
+        );
+
+        const call = jest.spyOn(messenger, 'call');
+        messenger.call('SnapController:init');
+        await sleep(10);
+
+        expect(call).toHaveBeenNthCalledWith(
+          2,
+          'PermissionController:hasPermission',
+          MOCK_SNAP_ID,
+          'endowment:lifecycle-hooks',
+        );
+
+        expect(call).toHaveBeenNthCalledWith(
+          6,
+          'ExecutionService:executeSnap',
+          expect.any(Object),
+        );
+
+        expect(messenger.call).toHaveBeenNthCalledWith(
+          7,
+          'ExecutionService:handleRpcRequest',
+          MOCK_SNAP_ID,
+          {
+            handler: HandlerType.OnStart,
+            origin: METAMASK_ORIGIN,
+            request: {
+              jsonrpc: '2.0',
+              id: expect.any(String),
+              method: HandlerType.OnStart,
+            },
+          },
+        );
+
+        snapController.destroy();
+      });
+
+      it('logs an error if the lifecycle hook throws', async () => {
+        const consoleErrorSpy = jest
+          .spyOn(console, 'error')
+          .mockImplementation();
+
+        const rootMessenger = getControllerMessenger();
+        const messenger = getSnapControllerMessenger(rootMessenger);
+
+        rootMessenger.registerActionHandler(
+          'PermissionController:getPermissions',
+          () => {
+            return {
+              [SnapEndowments.LifecycleHooks]: MOCK_LIFECYCLE_HOOKS_PERMISSION,
+            };
+          },
+        );
+
+        rootMessenger.registerActionHandler(
+          'ExecutionService:handleRpcRequest',
+          () => {
+            throw new Error('Test error in lifecycle hook.');
+          },
+        );
+
+        const snapController = getSnapController(
+          getSnapControllerOptions({
+            messenger,
+            state: {
+              snaps: getPersistedSnapsState(),
+            },
+          }),
+        );
+
+        messenger.call('SnapController:init');
+        await sleep(10);
+
+        expect(consoleErrorSpy).toHaveBeenCalledWith(
+          `Error when calling \`onStart\` lifecycle hook for Snap "npm:@metamask/example-snap": Test error in lifecycle hook.`,
+        );
+
+        snapController.destroy();
+      });
+    });
+
     describe('SnapController:get', () => {
       it('gets a snap', () => {
         const messenger = getSnapControllerMessenger();
diff --git a/packages/snaps-controllers/src/snaps/SnapController.ts b/packages/snaps-controllers/src/snaps/SnapController.ts
index f0ac1fc1a4..a9ceec5ac4 100644
--- a/packages/snaps-controllers/src/snaps/SnapController.ts
+++ b/packages/snaps-controllers/src/snaps/SnapController.ts
@@ -338,6 +338,15 @@ type PendingApproval = {
 
 // Controller Messenger Actions
 
+/**
+ * Initialise the SnapController. This should be called after all controllers
+ * are created.
+ */
+export type SnapControllerInitAction = {
+  type: `${typeof controllerName}:init`;
+  handler: SnapController['init'];
+};
+
 /**
  * Gets the specified Snap from state.
  */
@@ -470,6 +479,7 @@ export type SnapControllerGetStateAction = ControllerGetStateAction<
 >;
 
 export type SnapControllerActions =
+  | SnapControllerInitAction
   | ClearSnapState
   | GetSnap
   | GetSnapState
@@ -1160,6 +1170,11 @@ export class SnapController extends BaseController<
    * actions.
    */
   #registerMessageHandlers(): void {
+    this.messagingSystem.registerActionHandler(
+      `${controllerName}:init`,
+      (...args) => this.init(...args),
+    );
+
     this.messagingSystem.registerActionHandler(
       `${controllerName}:clearSnapState`,
       (...args) => this.clearSnapState(...args),
@@ -1266,6 +1281,37 @@ export class SnapController extends BaseController<
     );
   }
 
+  /**
+   * Initialise the SnapController.
+   *
+   * Currently this method calls the `onStart` lifecycle hook for all
+   * installed Snaps.
+   */
+  init() {
+    const snaps = this.getRunnableSnaps();
+    for (const { id } of snaps) {
+      const hasLifecycleHooksEndowment = this.messagingSystem.call(
+        'PermissionController:hasPermission',
+        id,
+        SnapEndowments.LifecycleHooks,
+      );
+
+      if (!hasLifecycleHooksEndowment) {
+        continue;
+      }
+
+      this.#callLifecycleHook(METAMASK_ORIGIN, id, HandlerType.OnStart).catch(
+        (error) => {
+          logError(
+            `Error when calling \`onStart\` lifecycle hook for Snap "${id}": ${getErrorMessage(
+              error,
+            )}`,
+          );
+        },
+      );
+    }
+  }
+
   #handlePreinstalledSnaps(preinstalledSnaps: PreinstalledSnap[]) {
     for (const {
       snapId,
diff --git a/packages/snaps-execution-environments/coverage.json b/packages/snaps-execution-environments/coverage.json
index bc6a469604..e4e7ddfae4 100644
--- a/packages/snaps-execution-environments/coverage.json
+++ b/packages/snaps-execution-environments/coverage.json
@@ -1,6 +1,6 @@
 {
-  "branches": 90,
+  "branches": 90.04,
   "functions": 94.69,
-  "lines": 90.41,
+  "lines": 90.42,
   "statements": 89.62
 }
diff --git a/packages/snaps-execution-environments/src/common/BaseSnapExecutor.test.browser.ts b/packages/snaps-execution-environments/src/common/BaseSnapExecutor.test.browser.ts
index 32d17c0af1..b81728db3b 100644
--- a/packages/snaps-execution-environments/src/common/BaseSnapExecutor.test.browser.ts
+++ b/packages/snaps-execution-environments/src/common/BaseSnapExecutor.test.browser.ts
@@ -1896,7 +1896,11 @@ describe('BaseSnapExecutor', () => {
   });
 
   describe('lifecycle hooks', () => {
-    const LIFECYCLE_HOOKS = [HandlerType.OnInstall, HandlerType.OnUpdate];
+    const LIFECYCLE_HOOKS = [
+      HandlerType.OnInstall,
+      HandlerType.OnUpdate,
+      HandlerType.OnStart,
+    ];
 
     for (const handler of LIFECYCLE_HOOKS) {
       it(`supports \`${handler}\` export`, async () => {
diff --git a/packages/snaps-execution-environments/src/common/commands.ts b/packages/snaps-execution-environments/src/common/commands.ts
index 68588a43f6..bc1c574248 100644
--- a/packages/snaps-execution-environments/src/common/commands.ts
+++ b/packages/snaps-execution-environments/src/common/commands.ts
@@ -120,6 +120,7 @@ export function getHandlerArguments(
 
     case HandlerType.OnInstall:
     case HandlerType.OnUpdate:
+    case HandlerType.OnStart:
       return { origin };
 
     case HandlerType.OnHomePage:
diff --git a/packages/snaps-jest/src/helpers.ts b/packages/snaps-jest/src/helpers.ts
index 2300147be5..42d8cfe27c 100644
--- a/packages/snaps-jest/src/helpers.ts
+++ b/packages/snaps-jest/src/helpers.ts
@@ -187,6 +187,7 @@ export async function installSnap<
     onKeyringRequest,
     onInstall,
     onUpdate,
+    onStart,
     onNameLookup,
     onProtocolRequest,
     onClientRequest,
@@ -208,6 +209,7 @@ export async function installSnap<
     onKeyringRequest,
     onInstall,
     onUpdate,
+    onStart,
     onNameLookup,
     onProtocolRequest,
     onClientRequest,
diff --git a/packages/snaps-rpc-methods/src/endowments/index.ts b/packages/snaps-rpc-methods/src/endowments/index.ts
index 5730bea959..c656c73a9e 100644
--- a/packages/snaps-rpc-methods/src/endowments/index.ts
+++ b/packages/snaps-rpc-methods/src/endowments/index.ts
@@ -121,6 +121,7 @@ export const handlerEndowments: Record<HandlerType, string | null> = {
   [HandlerType.OnNameLookup]: nameLookupEndowmentBuilder.targetName,
   [HandlerType.OnInstall]: lifecycleHooksEndowmentBuilder.targetName,
   [HandlerType.OnUpdate]: lifecycleHooksEndowmentBuilder.targetName,
+  [HandlerType.OnStart]: lifecycleHooksEndowmentBuilder.targetName,
   [HandlerType.OnKeyringRequest]: keyringEndowmentBuilder.targetName,
   [HandlerType.OnHomePage]: homePageEndowmentBuilder.targetName,
   [HandlerType.OnSettingsPage]: settingsPageEndowmentBuilder.targetName,
diff --git a/packages/snaps-sdk/src/types/handlers/lifecycle.ts b/packages/snaps-sdk/src/types/handlers/lifecycle.ts
index 80585a3fc5..f047bd013b 100644
--- a/packages/snaps-sdk/src/types/handlers/lifecycle.ts
+++ b/packages/snaps-sdk/src/types/handlers/lifecycle.ts
@@ -37,3 +37,16 @@ export type OnInstallHandler = LifecycleEventHandler;
  * @param args.origin - The origin that triggered the lifecycle event hook.
  */
 export type OnUpdateHandler = LifecycleEventHandler;
+
+/**
+ * The `onStart` handler. This is called when the client is started.
+ *
+ * Note that using this handler requires the `endowment:lifecycle-hooks`
+ * permission.
+ *
+ * This type is an alias for {@link LifecycleEventHandler}.
+ *
+ * @param args - The request arguments.
+ * @param args.origin - The origin that triggered the lifecycle event hook.
+ */
+export type OnStartHandler = LifecycleEventHandler;
diff --git a/packages/snaps-simulation/src/helpers.test.tsx b/packages/snaps-simulation/src/helpers.test.tsx
index 74dcb839ca..7a88596093 100644
--- a/packages/snaps-simulation/src/helpers.test.tsx
+++ b/packages/snaps-simulation/src/helpers.test.tsx
@@ -701,6 +701,32 @@ describe('helpers', () => {
     });
   });
 
+  describe('onStart', () => {
+    it('sends a onStart request and returns the result', async () => {
+      jest.spyOn(console, 'log').mockImplementation();
+
+      const { snapId, close: closeServer } = await getMockServer({
+        sourceCode: `
+          module.exports.onStart = async () => {
+            return { content: { type: 'text', value: 'Hello, world!' } };
+          };
+         `,
+      });
+
+      const { onStart, close } = await installSnap(snapId);
+      const response = await onStart();
+
+      expect(response).toStrictEqual(
+        expect.objectContaining({
+          getInterface: expect.any(Function),
+        }),
+      );
+
+      await close();
+      await closeServer();
+    });
+  });
+
   describe('onProtocolRequest', () => {
     it('sends a onProtocolRequest request and returns the result', async () => {
       jest.spyOn(console, 'log').mockImplementation();
diff --git a/packages/snaps-simulation/src/helpers.ts b/packages/snaps-simulation/src/helpers.ts
index 889e2ba3f8..fc976ff60c 100644
--- a/packages/snaps-simulation/src/helpers.ts
+++ b/packages/snaps-simulation/src/helpers.ts
@@ -158,6 +158,13 @@ export type SnapHelpers = {
    */
   onUpdate(request?: Pick<RequestOptions, 'origin'>): SnapRequest;
 
+  /**
+   * Get the response from the Snap's `onStart` handler.
+   *
+   * @returns The response.
+   */
+  onStart(request?: Pick<RequestOptions, 'origin'>): SnapRequest;
+
   /**
    * Get the response from the Snap's `onNameLookup` handler.
    *
@@ -368,6 +375,25 @@ export function getHelpers({
       });
     },
 
+    // This can't be async because it returns a `SnapRequest`.
+    // eslint-disable-next-line @typescript-eslint/promise-function-async
+    onStart: (request?: Pick<RequestOptions, 'origin'>) => {
+      log('Running onStart handler.');
+
+      return handleRequest({
+        snapId,
+        store,
+        executionService,
+        controllerMessenger,
+        runSaga,
+        handler: HandlerType.OnStart,
+        request: {
+          method: '',
+          ...request,
+        },
+      });
+    },
+
     onNameLookup: async (
       nameLookupOptions: NameLookupOptions,
     ): Promise<SnapResponseWithoutInterface> => {
diff --git a/packages/snaps-simulation/src/types.ts b/packages/snaps-simulation/src/types.ts
index 37aa907730..73dec241bb 100644
--- a/packages/snaps-simulation/src/types.ts
+++ b/packages/snaps-simulation/src/types.ts
@@ -492,6 +492,13 @@ export type Snap = {
    */
   onUpdate(request?: Pick<RequestOptions, 'origin'>): SnapRequest;
 
+  /**
+   * Get the response from the Snap's `onStart` handler.
+   *
+   * @returns The response.
+   */
+  onStart(request?: Pick<RequestOptions, 'origin'>): SnapRequest;
+
   /**
    * Get the response from the Snap's `onNameLookup` handler.
    *
diff --git a/packages/snaps-utils/coverage.json b/packages/snaps-utils/coverage.json
index e800862e07..5eee8de081 100644
--- a/packages/snaps-utils/coverage.json
+++ b/packages/snaps-utils/coverage.json
@@ -1,6 +1,6 @@
 {
   "branches": 99.76,
-  "functions": 99,
+  "functions": 99.01,
   "lines": 98.69,
   "statements": 97.29
 }
diff --git a/packages/snaps-utils/src/handlers/exports.test.ts b/packages/snaps-utils/src/handlers/exports.test.ts
index 8a0b081846..a89da358b8 100644
--- a/packages/snaps-utils/src/handlers/exports.test.ts
+++ b/packages/snaps-utils/src/handlers/exports.test.ts
@@ -21,6 +21,7 @@ describe('SNAP_EXPORT_NAMES', () => {
       'onCronjob',
       'onInstall',
       'onUpdate',
+      'onStart',
       'onNameLookup',
       'onKeyringRequest',
       'onHomePage',
diff --git a/packages/snaps-utils/src/handlers/exports.ts b/packages/snaps-utils/src/handlers/exports.ts
index 656e79d3de..82aaf19de1 100644
--- a/packages/snaps-utils/src/handlers/exports.ts
+++ b/packages/snaps-utils/src/handlers/exports.ts
@@ -12,6 +12,7 @@ import type {
   OnRpcRequestHandler,
   OnSettingsPageHandler,
   OnSignatureHandler,
+  OnStartHandler,
   OnTransactionHandler,
   OnUpdateHandler,
   OnUserInputHandler,
@@ -63,6 +64,13 @@ export const SNAP_EXPORTS = {
       return typeof snapExport === 'function';
     },
   },
+  [HandlerType.OnStart]: {
+    type: HandlerType.OnStart,
+    required: false,
+    validator: (snapExport: unknown): snapExport is OnStartHandler => {
+      return typeof snapExport === 'function';
+    },
+  },
   [HandlerType.OnKeyringRequest]: {
     type: HandlerType.OnKeyringRequest,
     required: true,
diff --git a/packages/snaps-utils/src/handlers/types.ts b/packages/snaps-utils/src/handlers/types.ts
index 371e7932a8..af3ad495f8 100644
--- a/packages/snaps-utils/src/handlers/types.ts
+++ b/packages/snaps-utils/src/handlers/types.ts
@@ -35,6 +35,7 @@ export enum HandlerType {
   OnCronjob = 'onCronjob',
   OnInstall = 'onInstall',
   OnUpdate = 'onUpdate',
+  OnStart = 'onStart',
   OnNameLookup = 'onNameLookup',
   OnKeyringRequest = 'onKeyringRequest',
   OnHomePage = 'onHomePage',