diff --git a/eslint-suppressions.json b/eslint-suppressions.json
index 1d41465cfa..0e0cf97028 100644
--- a/eslint-suppressions.json
+++ b/eslint-suppressions.json
@@ -2239,7 +2239,7 @@
   },
   "packages/transaction-pay-controller/src/utils/transaction.ts": {
     "no-restricted-syntax": {
-      "count": 2
+      "count": 6
     }
   },
   "packages/user-operation-controller/src/UserOperationController.test.ts": {
diff --git a/packages/transaction-pay-controller/CHANGELOG.md b/packages/transaction-pay-controller/CHANGELOG.md
index c9bea4df38..e1e1a72ea1 100644
--- a/packages/transaction-pay-controller/CHANGELOG.md
+++ b/packages/transaction-pay-controller/CHANGELOG.md
@@ -9,6 +9,9 @@ and this project adheres to [Semantic Versioning](https://semver.org/spec/v2.0.0
 
 ### Changed
 
+- **BREAKING:** Re-parse required tokens when asset state changes ([#8714](https://github.com/MetaMask/core/pull/8714))
+  - Adds `AssetsControllerStateChangeEvent`, `CurrencyRateStateChange`, `TokenRatesControllerStateChangeEvent`, and `TokensControllerStateChangeEvent` to `AllowedEvents`.
+  - Consumers must grant these events when creating the controller messenger.
 - Bump `@metamask/gas-fee-controller` from `^26.1.1` to `^26.2.0` ([#8722](https://github.com/MetaMask/core/pull/8722))
 - Bump `@metamask/transaction-controller` from `^65.1.0` to `^65.2.0` ([#8722](https://github.com/MetaMask/core/pull/8722))
 
diff --git a/packages/transaction-pay-controller/src/TransactionPayController.test.ts b/packages/transaction-pay-controller/src/TransactionPayController.test.ts
index 1e18803732..e857a98390 100644
--- a/packages/transaction-pay-controller/src/TransactionPayController.test.ts
+++ b/packages/transaction-pay-controller/src/TransactionPayController.test.ts
@@ -17,7 +17,11 @@ import type {
 import { getStrategyOrder } from './utils/feature-flags';
 import { updateQuotes } from './utils/quotes';
 import { updateSourceAmounts } from './utils/source-amounts';
-import { getTransaction, pollTransactionChanges } from './utils/transaction';
+import {
+  getTransaction,
+  subscribeAssetChanges,
+  subscribeTransactionChanges,
+} from './utils/transaction';
 
 jest.mock('./actions/update-fiat-payment');
 jest.mock('./actions/update-payment-token');
@@ -41,7 +45,10 @@ describe('TransactionPayController', () => {
   const getTransactionMock = jest.mocked(getTransaction);
   const updateSourceAmountsMock = jest.mocked(updateSourceAmounts);
   const updateQuotesMock = jest.mocked(updateQuotes);
-  const pollTransactionChangesMock = jest.mocked(pollTransactionChanges);
+  const subscribeTransactionChangesMock = jest.mocked(
+    subscribeTransactionChanges,
+  );
+  const subscribeAssetChangesMock = jest.mocked(subscribeAssetChanges);
   const getStrategyOrderMock = jest.mocked(getStrategyOrder);
   let messenger: TransactionPayControllerMessenger;
   let getKeyringControllerStateMock: jest.Mock;
@@ -80,6 +87,21 @@ describe('TransactionPayController', () => {
     updateQuotesMock.mockResolvedValue(true);
   });
 
+  describe('constructor', () => {
+    it('subscribes to rate changes for in-flight retry', () => {
+      const controller = createController();
+
+      expect(subscribeAssetChangesMock).toHaveBeenCalledWith(
+        messenger,
+        expect.any(Function),
+        expect.any(Function),
+      );
+
+      const getControllerState = subscribeAssetChangesMock.mock.calls[0][1];
+      expect(getControllerState()).toBe(controller.state);
+    });
+  });
+
   describe('updatePaymentToken', () => {
     it('calls util', () => {
       createController().updatePaymentToken({
@@ -674,7 +696,7 @@ describe('TransactionPayController', () => {
       ).toBeDefined();
 
       const removeTransactionDataCallback =
-        pollTransactionChangesMock.mock.calls[0][2];
+        subscribeTransactionChangesMock.mock.calls[0][2];
 
       removeTransactionDataCallback(TRANSACTION_ID_MOCK);
 
diff --git a/packages/transaction-pay-controller/src/TransactionPayController.ts b/packages/transaction-pay-controller/src/TransactionPayController.ts
index 61cb6b4790..19d4fdfb6f 100644
--- a/packages/transaction-pay-controller/src/TransactionPayController.ts
+++ b/packages/transaction-pay-controller/src/TransactionPayController.ts
@@ -26,7 +26,11 @@ import type {
 import { getStrategyOrder } from './utils/feature-flags';
 import { updateQuotes } from './utils/quotes';
 import { updateSourceAmounts } from './utils/source-amounts';
-import { getTransaction, pollTransactionChanges } from './utils/transaction';
+import {
+  getTransaction,
+  subscribeAssetChanges,
+  subscribeTransactionChanges,
+} from './utils/transaction';
 
 const MESSENGER_EXPOSED_METHODS = [
   'getDelegationTransaction',
@@ -87,12 +91,18 @@ export class TransactionPayController extends BaseController<
       MESSENGER_EXPOSED_METHODS,
     );
 
-    pollTransactionChanges(
+    subscribeTransactionChanges(
       messenger,
       this.#updateTransactionData.bind(this),
       this.#removeTransactionData.bind(this),
     );
 
+    subscribeAssetChanges(
+      messenger,
+      () => this.state,
+      this.#updateTransactionData.bind(this),
+    );
+
     // eslint-disable-next-line no-new
     new QuoteRefresher({
       getStrategies: this.#getStrategiesWithFallback.bind(this),
diff --git a/packages/transaction-pay-controller/src/types.ts b/packages/transaction-pay-controller/src/types.ts
index 7c5064498e..d3ecc63e47 100644
--- a/packages/transaction-pay-controller/src/types.ts
+++ b/packages/transaction-pay-controller/src/types.ts
@@ -1,10 +1,18 @@
-import type { AssetsControllerGetStateForTransactionPayAction } from '@metamask/assets-controller';
+import type {
+  AssetsControllerGetStateForTransactionPayAction,
+  AssetsControllerStateChangeEvent,
+} from '@metamask/assets-controller';
 import type {
   CurrencyRateControllerGetStateAction,
+  CurrencyRateStateChange,
   TokenBalancesControllerGetStateAction,
 } from '@metamask/assets-controllers';
 import type { TokenRatesControllerGetStateAction } from '@metamask/assets-controllers';
-import type { TokensControllerGetStateAction } from '@metamask/assets-controllers';
+import type { TokenRatesControllerStateChangeEvent } from '@metamask/assets-controllers';
+import type {
+  TokensControllerGetStateAction,
+  TokensControllerStateChangeEvent,
+} from '@metamask/assets-controllers';
 import type { AccountTrackerControllerGetStateAction } from '@metamask/assets-controllers';
 import type { ControllerStateChangeEvent } from '@metamask/base-controller';
 import type { ControllerGetStateAction } from '@metamask/base-controller';
@@ -82,7 +90,11 @@ export type AllowedActions =
   | TransactionControllerUpdateTransactionAction;
 
 export type AllowedEvents =
+  | AssetsControllerStateChangeEvent
   | BridgeStatusControllerStateChangeEvent
+  | CurrencyRateStateChange
+  | TokenRatesControllerStateChangeEvent
+  | TokensControllerStateChangeEvent
   | TransactionControllerStateChangeEvent
   | TransactionControllerUnapprovedTransactionAddedEvent;
 
diff --git a/packages/transaction-pay-controller/src/utils/required-tokens.ts b/packages/transaction-pay-controller/src/utils/required-tokens.ts
index 93367c647b..9103a6c1ce 100644
--- a/packages/transaction-pay-controller/src/utils/required-tokens.ts
+++ b/packages/transaction-pay-controller/src/utils/required-tokens.ts
@@ -3,7 +3,9 @@ import { toHex } from '@metamask/controller-utils';
 import { abiERC20 } from '@metamask/metamask-eth-abis';
 import type { TransactionMeta } from '@metamask/transaction-controller';
 import type { Hex } from '@metamask/utils';
+import { createModuleLogger } from '@metamask/utils';
 
+import { projectLogger } from '../logger';
 import type {
   TransactionPayControllerMessenger,
   TransactionPayRequiredToken,
@@ -15,6 +17,8 @@ import {
   getTokenInfo,
 } from './token';
 
+const log = createModuleLogger(projectLogger, 'required-tokens');
+
 const FOUR_BYTE_TOKEN_TRANSFER = '0xa9059cbb';
 
 /**
@@ -61,19 +65,28 @@ function getTokenTransferToken(
   const { data, to } = getTokenTransferData(transaction) ?? {};
 
   if (!to || !data) {
+    log('No token transfer detected', {
+      transactionId: transaction.id,
+    });
     return undefined;
   }
 
   let transferAmount: Hex | undefined;
+  let decodeError: unknown;
 
   try {
     const result = new Interface(abiERC20).decodeFunctionData('transfer', data);
     transferAmount = toHex(result._value);
-  } catch {
-    // Intentionally empty
+  } catch (error) {
+    decodeError = error;
   }
 
   if (transferAmount === undefined) {
+    log('Failed to decode transfer calldata', {
+      transactionId: transaction.id,
+      to,
+      error: decodeError,
+    });
     return undefined;
   }
 
@@ -105,6 +118,16 @@ function buildRequiredToken(
   const tokenBalance = getTokenBalance(messenger, from, chainId, tokenAddress);
 
   if (tokenDecimals === undefined || !symbol || fiatRates === undefined) {
+    log('Missing token data', {
+      transactionId: transaction.id,
+      chainId,
+      tokenAddress,
+      missing: {
+        decimals: tokenDecimals === undefined,
+        symbol: !symbol,
+        fiatRates: fiatRates === undefined,
+      },
+    });
     return undefined;
   }
 
diff --git a/packages/transaction-pay-controller/src/utils/transaction.test.ts b/packages/transaction-pay-controller/src/utils/transaction.test.ts
index c24fbc5c62..c409c89670 100644
--- a/packages/transaction-pay-controller/src/utils/transaction.test.ts
+++ b/packages/transaction-pay-controller/src/utils/transaction.test.ts
@@ -8,18 +8,25 @@ import type { Hex } from '@metamask/utils';
 import { noop } from 'lodash';
 
 import { getMessengerMock } from '../tests/messenger-mock';
-import type { TransactionData, TransactionPayRequiredToken } from '../types';
+import type {
+  TransactionData,
+  TransactionPayControllerState,
+  TransactionPayRequiredToken,
+} from '../types';
+import { getAssetsUnifyStateFeature } from './feature-flags';
 import { parseRequiredTokens } from './required-tokens';
 import {
   FINALIZED_STATUSES,
   collectTransactionIds,
   getTransaction,
   isPredictWithdrawTransaction,
-  pollTransactionChanges,
+  subscribeAssetChanges,
+  subscribeTransactionChanges,
   updateTransaction,
   waitForTransactionConfirmed,
 } from './transaction';
 
+jest.mock('./feature-flags');
 jest.mock('./required-tokens');
 
 const TRANSACTION_ID_MOCK = '123-456';
@@ -44,6 +51,9 @@ const TRANSCTION_TOKEN_REQUIRED_MOCK = {
 
 describe('Transaction Utils', () => {
   const parseRequiredTokensMock = jest.mocked(parseRequiredTokens);
+  const getAssetsUnifyStateFeatureMock = jest.mocked(
+    getAssetsUnifyStateFeature,
+  );
   const {
     messenger,
     getTransactionControllerStateMock,
@@ -57,6 +67,8 @@ describe('Transaction Utils', () => {
     getTransactionControllerStateMock.mockReturnValue({
       transactions: [] as TransactionMeta[],
     } as TransactionControllerState);
+
+    getAssetsUnifyStateFeatureMock.mockReturnValue(false);
   });
 
   describe('getTransaction', () => {
@@ -79,13 +91,13 @@ describe('Transaction Utils', () => {
     });
   });
 
-  describe('pollTransactionChanges', () => {
+  describe('subscribeTransactionChanges', () => {
     it('updates state for new transactions', () => {
       const updateTransactionDataMock = jest.fn();
 
       parseRequiredTokensMock.mockReturnValue([TRANSCTION_TOKEN_REQUIRED_MOCK]);
 
-      pollTransactionChanges(messenger, updateTransactionDataMock, noop);
+      subscribeTransactionChanges(messenger, updateTransactionDataMock, noop);
 
       publish(
         'TransactionController:stateChange',
@@ -110,7 +122,7 @@ describe('Transaction Utils', () => {
 
       parseRequiredTokensMock.mockReturnValue([TRANSCTION_TOKEN_REQUIRED_MOCK]);
 
-      pollTransactionChanges(messenger, updateTransactionDataMock, noop);
+      subscribeTransactionChanges(messenger, updateTransactionDataMock, noop);
 
       publish(
         'TransactionController:stateChange',
@@ -138,7 +150,7 @@ describe('Transaction Utils', () => {
       (status) => {
         const removeTransactionDataMock = jest.fn();
 
-        pollTransactionChanges(messenger, noop, removeTransactionDataMock);
+        subscribeTransactionChanges(messenger, noop, removeTransactionDataMock);
 
         publish(
           'TransactionController:stateChange',
@@ -165,7 +177,7 @@ describe('Transaction Utils', () => {
     it('removes state if transaction is deleted', () => {
       const removeTransactionDataMock = jest.fn();
 
-      pollTransactionChanges(messenger, noop, removeTransactionDataMock);
+      subscribeTransactionChanges(messenger, noop, removeTransactionDataMock);
 
       publish(
         'TransactionController:stateChange',
@@ -189,6 +201,204 @@ describe('Transaction Utils', () => {
     });
   });
 
+  describe('subscribeAssetChanges', () => {
+    function buildState(
+      data: Partial<TransactionData> & {
+        tokens: TransactionPayRequiredToken[];
+      } = { tokens: [] },
+    ): TransactionPayControllerState {
+      return {
+        transactionData: {
+          [TRANSACTION_ID_MOCK]: {
+            isLoading: false,
+            ...data,
+          } as TransactionData,
+        },
+      };
+    }
+
+    let isolatedMessenger: ReturnType<typeof getMessengerMock>['messenger'];
+    let isolatedPublish: ReturnType<typeof getMessengerMock>['publish'];
+    let isolatedGetTransactionControllerStateMock: ReturnType<
+      typeof getMessengerMock
+    >['getTransactionControllerStateMock'];
+
+    beforeEach(() => {
+      const fresh = getMessengerMock();
+      isolatedMessenger = fresh.messenger;
+      isolatedPublish = fresh.publish;
+      isolatedGetTransactionControllerStateMock =
+        fresh.getTransactionControllerStateMock;
+      isolatedGetTransactionControllerStateMock.mockReturnValue({
+        transactions: [] as TransactionMeta[],
+      } as TransactionControllerState);
+    });
+
+    it('re-parses required tokens for transactions with empty tokens when token rates change', () => {
+      const updateTransactionDataMock = jest.fn();
+
+      parseRequiredTokensMock.mockReturnValue([TRANSCTION_TOKEN_REQUIRED_MOCK]);
+      isolatedGetTransactionControllerStateMock.mockReturnValue({
+        transactions: [TRANSACTION_META_MOCK],
+      } as TransactionControllerState);
+
+      subscribeAssetChanges(
+        isolatedMessenger,
+        () => buildState({ tokens: [] }),
+        updateTransactionDataMock,
+      );
+
+      isolatedPublish('TokenRatesController:stateChange', {} as never, []);
+
+      expect(updateTransactionDataMock).toHaveBeenCalledTimes(1);
+      const transactionData = {} as TransactionData;
+      updateTransactionDataMock.mock.calls[0][1](transactionData);
+      expect(transactionData.tokens).toStrictEqual([
+        TRANSCTION_TOKEN_REQUIRED_MOCK,
+      ]);
+    });
+
+    it('re-parses required tokens when currency rates change', () => {
+      const updateTransactionDataMock = jest.fn();
+
+      parseRequiredTokensMock.mockReturnValue([TRANSCTION_TOKEN_REQUIRED_MOCK]);
+      isolatedGetTransactionControllerStateMock.mockReturnValue({
+        transactions: [TRANSACTION_META_MOCK],
+      } as TransactionControllerState);
+
+      subscribeAssetChanges(
+        isolatedMessenger,
+        () => buildState({ tokens: [] }),
+        updateTransactionDataMock,
+      );
+
+      isolatedPublish('CurrencyRateController:stateChange', {} as never, []);
+
+      expect(updateTransactionDataMock).toHaveBeenCalledTimes(1);
+    });
+
+    it('re-parses required tokens when token state changes', () => {
+      const updateTransactionDataMock = jest.fn();
+
+      parseRequiredTokensMock.mockReturnValue([TRANSCTION_TOKEN_REQUIRED_MOCK]);
+      isolatedGetTransactionControllerStateMock.mockReturnValue({
+        transactions: [TRANSACTION_META_MOCK],
+      } as TransactionControllerState);
+
+      subscribeAssetChanges(
+        isolatedMessenger,
+        () => buildState({ tokens: [] }),
+        updateTransactionDataMock,
+      );
+
+      isolatedPublish('TokensController:stateChange', {} as never, []);
+
+      expect(updateTransactionDataMock).toHaveBeenCalledTimes(1);
+    });
+
+    it('subscribes to AssetsController state changes when unify-state feature is enabled', () => {
+      const updateTransactionDataMock = jest.fn();
+
+      getAssetsUnifyStateFeatureMock.mockReturnValue(true);
+      parseRequiredTokensMock.mockReturnValue([TRANSCTION_TOKEN_REQUIRED_MOCK]);
+      isolatedGetTransactionControllerStateMock.mockReturnValue({
+        transactions: [TRANSACTION_META_MOCK],
+      } as TransactionControllerState);
+
+      subscribeAssetChanges(
+        isolatedMessenger,
+        () => buildState({ tokens: [] }),
+        updateTransactionDataMock,
+      );
+
+      isolatedPublish('AssetsController:stateChange', {} as never, []);
+
+      expect(updateTransactionDataMock).toHaveBeenCalledTimes(1);
+    });
+
+    it('does not subscribe to per-source events when unify-state feature is enabled', () => {
+      const updateTransactionDataMock = jest.fn();
+
+      getAssetsUnifyStateFeatureMock.mockReturnValue(true);
+      isolatedGetTransactionControllerStateMock.mockReturnValue({
+        transactions: [TRANSACTION_META_MOCK],
+      } as TransactionControllerState);
+
+      subscribeAssetChanges(
+        isolatedMessenger,
+        () => buildState({ tokens: [] }),
+        updateTransactionDataMock,
+      );
+
+      isolatedPublish('TokensController:stateChange', {} as never, []);
+      isolatedPublish('TokenRatesController:stateChange', {} as never, []);
+      isolatedPublish('CurrencyRateController:stateChange', {} as never, []);
+
+      expect(updateTransactionDataMock).not.toHaveBeenCalled();
+    });
+
+    it('skips transactions whose tokens are already populated', () => {
+      const updateTransactionDataMock = jest.fn();
+
+      isolatedGetTransactionControllerStateMock.mockReturnValue({
+        transactions: [TRANSACTION_META_MOCK],
+      } as TransactionControllerState);
+
+      subscribeAssetChanges(
+        isolatedMessenger,
+        () =>
+          buildState({
+            tokens: [TRANSCTION_TOKEN_REQUIRED_MOCK],
+          }),
+        updateTransactionDataMock,
+      );
+
+      isolatedPublish('TokenRatesController:stateChange', {} as never, []);
+
+      expect(updateTransactionDataMock).not.toHaveBeenCalled();
+      expect(parseRequiredTokensMock).not.toHaveBeenCalled();
+    });
+
+    it.each(FINALIZED_STATUSES)(
+      'skips transactions whose status is %s',
+      (status) => {
+        const updateTransactionDataMock = jest.fn();
+
+        isolatedGetTransactionControllerStateMock.mockReturnValue({
+          transactions: [{ ...TRANSACTION_META_MOCK, status }],
+        } as TransactionControllerState);
+
+        subscribeAssetChanges(
+          isolatedMessenger,
+          () => buildState({ tokens: [] }),
+          updateTransactionDataMock,
+        );
+
+        isolatedPublish('TokenRatesController:stateChange', {} as never, []);
+
+        expect(updateTransactionDataMock).not.toHaveBeenCalled();
+      },
+    );
+
+    it('skips transactions that no longer exist in TransactionController state', () => {
+      const updateTransactionDataMock = jest.fn();
+
+      isolatedGetTransactionControllerStateMock.mockReturnValue({
+        transactions: [] as TransactionMeta[],
+      } as TransactionControllerState);
+
+      subscribeAssetChanges(
+        isolatedMessenger,
+        () => buildState({ tokens: [] }),
+        updateTransactionDataMock,
+      );
+
+      isolatedPublish('TokenRatesController:stateChange', {} as never, []);
+
+      expect(updateTransactionDataMock).not.toHaveBeenCalled();
+    });
+  });
+
   describe('updateTransaction', () => {
     it('updates transaction', () => {
       getTransactionControllerStateMock.mockReturnValue({
diff --git a/packages/transaction-pay-controller/src/utils/transaction.ts b/packages/transaction-pay-controller/src/utils/transaction.ts
index ee75e3a182..c97d4004ec 100644
--- a/packages/transaction-pay-controller/src/utils/transaction.ts
+++ b/packages/transaction-pay-controller/src/utils/transaction.ts
@@ -5,13 +5,16 @@ import {
 import type { TransactionMeta } from '@metamask/transaction-controller';
 import type { Hex } from '@metamask/utils';
 import { createModuleLogger } from '@metamask/utils';
+import type { Patch } from 'immer';
 import { cloneDeep } from 'lodash';
 
 import { projectLogger } from '../logger';
 import type {
   TransactionPayControllerMessenger,
+  TransactionPayControllerState,
   UpdateTransactionDataCallback,
 } from '../types';
+import { getAssetsUnifyStateFeature } from './feature-flags';
 import { parseRequiredTokens } from './required-tokens';
 
 const log = createModuleLogger(projectLogger, 'transaction');
@@ -43,13 +46,13 @@ export function getTransaction(
 }
 
 /**
- * Poll for transaction changes and update the transaction data accordingly.
+ * Subscribe to transaction changes and update the transaction data accordingly.
  *
  * @param messenger - Controller messenger.
  * @param updateTransactionData - Callback to update transaction data.
  * @param removeTransactionData - Callback to remove transaction data.
  */
-export function pollTransactionChanges(
+export function subscribeTransactionChanges(
   messenger: TransactionPayControllerMessenger,
   updateTransactionData: UpdateTransactionDataCallback,
   removeTransactionData: (transactionId: string) => void,
@@ -103,6 +106,63 @@ export function pollTransactionChanges(
   );
 }
 
+/**
+ * Subscribe to asset state changes and re-parse required tokens for
+ * in-flight transactions whose tokens have not yet resolved.
+ *
+ * @param messenger - Controller messenger.
+ * @param getControllerState - Callback returning the current controller state.
+ * @param updateTransactionData - Callback to update transaction data.
+ */
+export function subscribeAssetChanges(
+  messenger: TransactionPayControllerMessenger,
+  getControllerState: () => TransactionPayControllerState,
+  updateTransactionData: UpdateTransactionDataCallback,
+): void {
+  const buildHandler =
+    (source: string) =>
+    (_state: unknown, patches: Patch[] | undefined): void => {
+      const { transactionData } = getControllerState();
+
+      for (const [transactionId, data] of Object.entries(transactionData)) {
+        if (data.tokens.length > 0) {
+          continue;
+        }
+
+        const transaction = getTransaction(transactionId, messenger);
+
+        if (!transaction || FINALIZED_STATUSES.includes(transaction.status)) {
+          continue;
+        }
+
+        log('Asset data changed', { transactionId, source, patches });
+
+        onTransactionChange(transaction, messenger, updateTransactionData);
+      }
+    };
+
+  if (getAssetsUnifyStateFeature(messenger)) {
+    messenger.subscribe(
+      'AssetsController:stateChange',
+      buildHandler('AssetsController'),
+    );
+    return;
+  }
+
+  messenger.subscribe(
+    'TokensController:stateChange',
+    buildHandler('TokensController'),
+  );
+  messenger.subscribe(
+    'TokenRatesController:stateChange',
+    buildHandler('TokenRatesController'),
+  );
+  messenger.subscribe(
+    'CurrencyRateController:stateChange',
+    buildHandler('CurrencyRateController'),
+  );
+}
+
 /**
  * Wait for a transaction to be confirmed or fail.
  *