diff --git a/packages/snaps-controllers/src/snaps/SnapController.test.tsx b/packages/snaps-controllers/src/snaps/SnapController.test.tsx
index e75b5cf2f0..1b55c086c9 100644
--- a/packages/snaps-controllers/src/snaps/SnapController.test.tsx
+++ b/packages/snaps-controllers/src/snaps/SnapController.test.tsx
@@ -8092,7 +8092,17 @@ describe('SnapController', () => {
         })
       ).manifest.result;
 
-      const manifest2 = (
+      const manifest2Old = (
+        await getMockSnapFilesWithUpdatedChecksum({
+          manifest: getSnapManifest({
+            initialConnections: {
+              [MOCK_ORIGIN]: {},
+            },
+          }),
+        })
+      ).manifest.result;
+
+      const manifest2New = (
         await getMockSnapFilesWithUpdatedChecksum({
           manifest: getSnapManifest({
             version: newVersion,
@@ -8105,7 +8115,9 @@ describe('SnapController', () => {
       const detect = jest
         .fn()
         .mockImplementationOnce(() => new LoopbackLocation())
-        .mockImplementationOnce(() => new LoopbackLocation())
+        .mockImplementationOnce(
+          () => new LoopbackLocation({ manifest: manifest2Old }),
+        )
         .mockImplementationOnce(() => new LoopbackLocation())
         .mockImplementationOnce(
           () =>
@@ -8116,7 +8128,7 @@ describe('SnapController', () => {
         .mockImplementationOnce(
           () =>
             new LoopbackLocation({
-              manifest: manifest2,
+              manifest: manifest2New,
               files: [
                 new VirtualFile({
                   value: 'foo',
@@ -8130,8 +8142,46 @@ describe('SnapController', () => {
             }),
         );
 
+      const rootMessenger = getControllerMessenger();
+
+      let revokedConnection = false;
+
+      rootMessenger.registerActionHandler(
+        'PermissionController:revokePermissions',
+        () => {
+          revokedConnection = true;
+          return {};
+        },
+      );
+
+      rootMessenger.registerActionHandler(
+        'PermissionController:getPermissions',
+        (origin) => {
+          if (origin === MOCK_ORIGIN && !revokedConnection) {
+            return {
+              [WALLET_SNAP_PERMISSION_KEY]: {
+                caveats: [
+                  {
+                    type: SnapCaveatType.SnapIds,
+                    value: {
+                      [snapId2]: {},
+                    },
+                  },
+                ],
+                date: 1664187844588,
+                id: 'izn0WGUO8cvq_jqvLQuQP',
+                invoker: MOCK_ORIGIN,
+                parentCapability: WALLET_SNAP_PERMISSION_KEY,
+              },
+            };
+          }
+          return MOCK_SNAP_PERMISSIONS;
+        },
+      );
+
       const options = getSnapControllerWithEESOptions({
         detectSnapLocation: detect,
+        rootMessenger,
       });
 
       const { messenger } = options;
@@ -8176,6 +8226,34 @@ describe('SnapController', () => {
         expect.anything(),
       );
 
+      expect(messenger.call).toHaveBeenNthCalledWith(
+        48,
+        'PermissionController:revokePermissions',
+        {
+          [MOCK_ORIGIN]: [WALLET_SNAP_PERMISSION_KEY],
+        },
+      );
+
+      expect(messenger.call).toHaveBeenNthCalledWith(
+        59,
+        'PermissionController:grantPermissions',
+        {
+          approvedPermissions: {
+            [WALLET_SNAP_PERMISSION_KEY]: {
+              caveats: [
+                {
+                  type: SnapCaveatType.SnapIds,
+                  value: {
+                    [snapId2]: {},
+                  },
+                },
+              ],
+            },
+          },
+          subject: { origin: MOCK_ORIGIN },
+        },
+      );
+
       controller.destroy();
       await service.terminateAllSnaps();
     });
diff --git a/packages/snaps-controllers/src/snaps/SnapController.ts b/packages/snaps-controllers/src/snaps/SnapController.ts
index f490c70793..e9c32477d5 100644
--- a/packages/snaps-controllers/src/snaps/SnapController.ts
+++ b/packages/snaps-controllers/src/snaps/SnapController.ts
@@ -58,6 +58,7 @@ import type {
   OnAssetsMarketDataResponse,
   AssetMarketData,
   AssetMetadata,
+  EmptyObject,
 } from '@metamask/snaps-sdk';
 import {
   AuxiliaryFileEncoding,
@@ -333,6 +334,8 @@ type RollbackSnapshot = {
     granted?: RequestedPermissions;
     requestData?: Record<string, unknown>;
   };
+  previousInitialConnections?: Record<string, EmptyObject> | null;
+  newInitialConnections?: Record<string, EmptyObject>;
   newVersion: string;
 };
 
@@ -2994,19 +2997,22 @@ export class SnapController extends BaseController<
         requestData,
       });
 
-      if (manifest.initialConnections) {
-        this.#handleInitialConnections(
-          snapId,
-          oldManifest.initialConnections ?? null,
-          manifest.initialConnections,
-        );
-      }
+      const previousInitialConnections = oldManifest.initialConnections ?? null;
+      const newInitialConnections = manifest.initialConnections ?? {};
+      this.#handleInitialConnections(
+        snapId,
+        previousInitialConnections,
+        newInitialConnections,
+      );
 
       const rollbackSnapshot = this.#getRollbackSnapshot(snapId);
       if (rollbackSnapshot !== undefined) {
         rollbackSnapshot.permissions.revoked = unusedPermissions;
         rollbackSnapshot.permissions.granted = approvedNewPermissions;
         rollbackSnapshot.permissions.requestData = requestData;
+        rollbackSnapshot.previousInitialConnections =
+          previousInitialConnections;
+        rollbackSnapshot.newInitialConnections = newInitialConnections;
       }
 
       const sourceCode = sourceCodeFile.toString();
@@ -4139,7 +4145,12 @@ export class SnapController extends BaseController<
       this.#transition(snapId, SnapStatusEvents.Stop);
     }
 
-    const { statePatches, permissions } = rollbackSnapshot;
+    const {
+      statePatches,
+      permissions,
+      previousInitialConnections,
+      newInitialConnections,
+    } = rollbackSnapshot;
 
     if (statePatches?.length) {
       this.applyPatches(statePatches);
@@ -4160,6 +4171,13 @@ export class SnapController extends BaseController<
       requestData: permissions.requestData,
     });
 
+    // Calling this in reverse order to undo the changes
+    this.#handleInitialConnections(
+      snapId,
+      newInitialConnections ?? null,
+      previousInitialConnections ?? {},
+    );
+
     const truncatedSnap = this.getTruncatedExpect(snapId);
 
     this.messagingSystem.publish(