diff --git a/packages/transaction-pay-controller/CHANGELOG.md b/packages/transaction-pay-controller/CHANGELOG.md
index f1e60db0bd..dc46544f20 100644
--- a/packages/transaction-pay-controller/CHANGELOG.md
+++ b/packages/transaction-pay-controller/CHANGELOG.md
@@ -45,6 +45,7 @@ and this project adheres to [Semantic Versioning](https://semver.org/spec/v2.0.0
 - Abort in-flight quote requests when a newer request is made for the same transaction, preventing stale responses from overwriting newer ones ([#8612](https://github.com/MetaMask/core/pull/8612))
 - Bump `@metamask/messenger` from `^1.1.1` to `^1.2.0` ([#8632](https://github.com/MetaMask/core/pull/8632))
 - Bump `@metamask/network-controller` from `^30.0.1` to `^30.1.0` ([#8636](https://github.com/MetaMask/core/pull/8636))
+- Fix post-quote relay submission when `accountOverride` is set by replacing the prepended original transaction with a delegation transaction so the override account can submit it ([#8615](https://github.com/MetaMask/core/pull/8615))
 
 ## [20.0.1]
 
diff --git a/packages/transaction-pay-controller/src/strategy/relay/relay-submit.test.ts b/packages/transaction-pay-controller/src/strategy/relay/relay-submit.test.ts
index f93a005c20..eb47e5a6a0 100644
--- a/packages/transaction-pay-controller/src/strategy/relay/relay-submit.test.ts
+++ b/packages/transaction-pay-controller/src/strategy/relay/relay-submit.test.ts
@@ -1013,6 +1013,73 @@ describe('Relay Submit Utils', () => {
         );
       });
 
+      describe('with accountOverride', () => {
+        const ACCOUNT_OVERRIDE_MOCK = '0xaccountOverride' as Hex;
+        const DELEGATION_TO_MOCK = '0xdelegationManager' as Hex;
+        const DELEGATION_DATA_MOCK = '0xdelegationdata' as Hex;
+        const DELEGATION_VALUE_MOCK = '0x0' as Hex;
+
+        beforeEach(() => {
+          request.quotes[0].request.from = ACCOUNT_OVERRIDE_MOCK;
+          getDelegationTransactionMock.mockResolvedValue({
+            data: DELEGATION_DATA_MOCK,
+            to: DELEGATION_TO_MOCK,
+            value: DELEGATION_VALUE_MOCK,
+          });
+        });
+
+        it('passes the original transaction through to getDelegationTransaction', async () => {
+          await submitRelayQuotes(request);
+
+          expect(getDelegationTransactionMock).toHaveBeenCalledTimes(1);
+          expect(getDelegationTransactionMock).toHaveBeenCalledWith({
+            transaction: expect.objectContaining({
+              id: ORIGINAL_TRANSACTION_ID_MOCK,
+              txParams: expect.objectContaining({
+                from: FROM_MOCK,
+                to: '0xrecipient',
+                data: '0xorigdata',
+                value: '0x100',
+              }),
+            }),
+          });
+        });
+
+        it('uses the delegation result as the first batch tx', async () => {
+          await submitRelayQuotes(request);
+
+          expect(addTransactionBatchMock).toHaveBeenCalledTimes(1);
+          expect(addTransactionBatchMock).toHaveBeenCalledWith(
+            expect.objectContaining({
+              from: ACCOUNT_OVERRIDE_MOCK,
+              transactions: [
+                expect.objectContaining({
+                  params: expect.objectContaining({
+                    data: DELEGATION_DATA_MOCK,
+                    to: DELEGATION_TO_MOCK,
+                    value: DELEGATION_VALUE_MOCK,
+                  }),
+                  type: TransactionType.simpleSend,
+                }),
+                expect.objectContaining({
+                  params: expect.objectContaining({
+                    data: '0x1234',
+                    to: '0xfedcb',
+                  }),
+                  type: TransactionType.relayDeposit,
+                }),
+              ],
+            }),
+          );
+        });
+      });
+
+      it('does not call getDelegationTransaction when accountOverride is not set', async () => {
+        await submitRelayQuotes(request);
+
+        expect(getDelegationTransactionMock).not.toHaveBeenCalled();
+      });
+
       it('activates 7702 mode with single combined post-quote gas limit', async () => {
         request.quotes[0].original.metamask.gasLimits = [203093];
         request.quotes[0].original.metamask.is7702 = true;
diff --git a/packages/transaction-pay-controller/src/strategy/relay/relay-submit.ts b/packages/transaction-pay-controller/src/strategy/relay/relay-submit.ts
index 0082b6af66..53165cb4af 100644
--- a/packages/transaction-pay-controller/src/strategy/relay/relay-submit.ts
+++ b/packages/transaction-pay-controller/src/strategy/relay/relay-submit.ts
@@ -343,20 +343,29 @@ async function submitTransactions(
   // For post-quote flows, prepend the original transaction so it gets
   // included in the batch alongside the relay deposit(s).
   // This always results in multiple params, so it takes the batch path.
+  // When an accountOverride is set (detected by `from` divergence between the
+  // quote and the original tx), the override account does not directly hold
+  // the funds for the original call, so the prepended tx is replaced with a
+  // delegation tx that redeems the original call on its behalf.
   const { isPostQuote } = quote.request;
-
-  const allParams =
-    isPostQuote && transaction.txParams.to
-      ? [
-          {
-            data: transaction.txParams.data as Hex | undefined,
-            from: transaction.txParams.from,
-            to: transaction.txParams.to,
-            value: transaction.txParams.value as Hex | undefined,
-          } as TransactionParams,
-          ...normalizedParams,
-        ]
-      : normalizedParams;
+  const hasAccountOverride =
+    quote.request.from.toLowerCase() !==
+    (transaction.txParams.from as Hex).toLowerCase();
+
+  let allParams = normalizedParams;
+
+  if (isPostQuote && transaction.txParams.to) {
+    const prependedParams = hasAccountOverride
+      ? await buildDelegatedOriginalParams(transaction, messenger)
+      : ({
+          data: transaction.txParams.data as Hex | undefined,
+          from: transaction.txParams.from,
+          to: transaction.txParams.to,
+          value: transaction.txParams.value as Hex | undefined,
+        } as TransactionParams);
+
+    allParams = [prependedParams, ...normalizedParams];
+  }
 
   if (quote.original.metamask.isExecute) {
     return await submitViaRelayExecute(
@@ -376,6 +385,38 @@ async function submitTransactions(
   );
 }
 
+/**
+ * Build TransactionParams for a delegation that redeems the original
+ * post-quote transaction on behalf of the override account. Used when the
+ * override account cannot execute the original call directly.
+ *
+ * The original tx is already on the correct chain and from the money
+ * account, so it can be passed through to `getDelegationTransaction`
+ * unchanged.
+ *
+ * @param transaction - Original transaction meta to be redeemed.
+ * @param messenger - Controller messenger.
+ * @returns Transaction params for the delegation tx.
+ */
+async function buildDelegatedOriginalParams(
+  transaction: TransactionMeta,
+  messenger: TransactionPayControllerMessenger,
+): Promise<TransactionParams> {
+  const delegation = await messenger.call(
+    'TransactionPayController:getDelegationTransaction',
+    { transaction },
+  );
+
+  log('Delegation result for prepended original tx', delegation);
+
+  return {
+    data: delegation.data,
+    from: transaction.txParams.from as Hex,
+    to: delegation.to,
+    value: delegation.value,
+  };
+}
+
 /**
  * Submit source transactions via Relay's /execute endpoint.
  *