diff --git a/packages/transaction-controller/CHANGELOG.md b/packages/transaction-controller/CHANGELOG.md
index 1bff4d745e..58772de962 100644
--- a/packages/transaction-controller/CHANGELOG.md
+++ b/packages/transaction-controller/CHANGELOG.md
@@ -11,6 +11,10 @@ and this project adheres to [Semantic Versioning](https://semver.org/spec/v2.0.0
 
 - Bump `@metamask/accounts-controller` from `^39.0.7` to `^39.1.0` ([#9807](https://github.com/MetaMask/core/pull/9807))
 
+### Fixed
+
+- Skip resimulation check when failing incomplete transactions at startup, preventing a crash when `isSimulationEnabled` depends on controllers not yet registered ([#9821](https://github.com/MetaMask/core/pull/9821))
+
 ## [69.5.1]
 
 ### Changed
diff --git a/packages/transaction-controller/src/TransactionController.test.ts b/packages/transaction-controller/src/TransactionController.test.ts
index 97a14a14ea..dbbc422a42 100644
--- a/packages/transaction-controller/src/TransactionController.test.ts
+++ b/packages/transaction-controller/src/TransactionController.test.ts
@@ -1275,6 +1275,55 @@ describe('TransactionController', () => {
       );
     });
 
+    it('fails signed transactions even when isSimulationEnabled throws', async () => {
+      const mockTransactionMeta = {
+        from: ACCOUNT_MOCK,
+        txParams: {
+          from: ACCOUNT_MOCK,
+          to: ACCOUNT_2_MOCK,
+        },
+      };
+
+      const mockedTransactions = [
+        {
+          id: '111',
+          chainId: toHex(5),
+          status: TransactionStatus.signed,
+          ...mockTransactionMeta,
+        },
+        {
+          id: '222',
+          chainId: toHex(1),
+          status: TransactionStatus.approved,
+          ...mockTransactionMeta,
+        },
+      ];
+
+      const mockedControllerState = {
+        transactions: mockedTransactions,
+        methodData: {},
+        lastFetchedBlockNumbers: {},
+      };
+
+      const { controller } = setupController({
+        options: {
+          isSimulationEnabled: () => {
+            throw new Error('Handler not registered');
+          },
+          // TODO: Replace `any` with type
+          // eslint-disable-next-line @typescript-eslint/no-explicit-any
+          state: mockedControllerState as any,
+        },
+      });
+
+      await flushPromises();
+
+      const { transactions } = controller.state;
+
+      expect(transactions[0].status).toBe(TransactionStatus.failed);
+      expect(transactions[1].status).toBe(TransactionStatus.failed);
+    });
+
     it('removes unapproved transactions', async () => {
       const mockTransactionMeta = {
         from: ACCOUNT_MOCK,
diff --git a/packages/transaction-controller/src/TransactionController.ts b/packages/transaction-controller/src/TransactionController.ts
index 244a0318ee..f6aa336639 100644
--- a/packages/transaction-controller/src/TransactionController.ts
+++ b/packages/transaction-controller/src/TransactionController.ts
@@ -4388,6 +4388,7 @@ export class TransactionController extends BaseController<
         {
           transactionId: transactionMeta.id,
           skipValidation: true,
+          skipResimulateCheck: true,
         },
         (draftTransactionMeta) => {
           draftTransactionMeta.status = TransactionStatus.failed;