diff --git a/packages/transaction-pay-controller/CHANGELOG.md b/packages/transaction-pay-controller/CHANGELOG.md
index abe28115cc..a8c46dd5da 100644
--- a/packages/transaction-pay-controller/CHANGELOG.md
+++ b/packages/transaction-pay-controller/CHANGELOG.md
@@ -11,6 +11,11 @@ and this project adheres to [Semantic Versioning](https://semver.org/spec/v2.0.0
 
 - Bump `@metamask/network-controller` from `^35.0.0` to `^35.0.1` ([#9758](https://github.com/MetaMask/core/pull/9758))
 
+### Fixed
+
+- Request `EXACT_OUTPUT` instead of `EXPECTED_OUTPUT` from Relay for HyperCore perps deposits, so the full deposit target is guaranteed to arrive ([#9751](https://github.com/MetaMask/core/pull/9751))
+  - `EXPECTED_OUTPUT` only guarantees `target * (1 - slippage)` on the destination, so a deposit sized to the exact margin required could arrive short and the follow-on order would fail with insufficient margin.
+
 ## [26.2.0]
 
 ### Changed
diff --git a/packages/transaction-pay-controller/src/strategy/relay/relay-quotes.test.ts b/packages/transaction-pay-controller/src/strategy/relay/relay-quotes.test.ts
index 69ee629ae4..93a32cf364 100644
--- a/packages/transaction-pay-controller/src/strategy/relay/relay-quotes.test.ts
+++ b/packages/transaction-pay-controller/src/strategy/relay/relay-quotes.test.ts
@@ -3913,6 +3913,58 @@ describe('Relay Quotes Utils', () => {
       );
     });
 
+    // A HyperCore deposit funds an order that needs the whole target as margin.
+    // EXPECTED_OUTPUT only guarantees `target * (1 - slippage)`, which leaves the
+    // follow-on order short and it fails on insufficient margin.
+    it('requests an exact output for Hyperliquid deposits so the full margin is guaranteed', async () => {
+      const arbitrumToHyperliquidRequest: QuoteRequest = {
+        ...QUOTE_REQUEST_MOCK,
+        targetChainId: CHAIN_ID_ARBITRUM,
+        targetTokenAddress: ARBITRUM_USDC_ADDRESS,
+      };
+
+      successfulFetchMock.mockResolvedValue({
+        ok: true,
+        json: async () => QUOTE_MOCK,
+      } as never);
+
+      await getRelayQuotes({
+        accountSupports7702: true,
+        messenger,
+        requests: [arbitrumToHyperliquidRequest],
+        transaction: {
+          ...TRANSACTION_META_MOCK,
+          type: TransactionType.perpsDepositAndOrder,
+        },
+      });
+
+      const body = JSON.parse(
+        successfulFetchMock.mock.calls[0][1]?.body as string,
+      );
+
+      expect(body.tradeType).toBe('EXACT_OUTPUT');
+    });
+
+    it('still requests an expected output for non-Hyperliquid targets', async () => {
+      successfulFetchMock.mockResolvedValue({
+        ok: true,
+        json: async () => QUOTE_MOCK,
+      } as never);
+
+      await getRelayQuotes({
+        accountSupports7702: true,
+        messenger,
+        requests: [QUOTE_REQUEST_MOCK],
+        transaction: TRANSACTION_META_MOCK,
+      });
+
+      const body = JSON.parse(
+        successfulFetchMock.mock.calls[0][1]?.body as string,
+      );
+
+      expect(body.tradeType).toBe('EXPECTED_OUTPUT');
+    });
+
     it('does not convert to Hyperliquid deposit when parent transaction is not a Perps deposit', async () => {
       const arbitrumUsdcRequest: QuoteRequest = {
         ...QUOTE_REQUEST_MOCK,
diff --git a/packages/transaction-pay-controller/src/strategy/relay/relay-quotes.ts b/packages/transaction-pay-controller/src/strategy/relay/relay-quotes.ts
index faf4047081..3cf47e3859 100644
--- a/packages/transaction-pay-controller/src/strategy/relay/relay-quotes.ts
+++ b/packages/transaction-pay-controller/src/strategy/relay/relay-quotes.ts
@@ -309,6 +309,12 @@ async function getSingleQuote(
     // eslint-disable-next-line @typescript-eslint/prefer-nullish-coalescing
     const useExactInput = isMaxAmount || request.isPostQuote;
 
+    // HyperCore perps deposits fund an order that requires the full target as
+    // margin, so the delivered amount must be guaranteed rather than expected.
+    // EXPECTED_OUTPUT only guarantees `target * (1 - slippage)`, which leaves
+    // the follow-on order short and it fails on insufficient margin.
+    const useExactOutput = !useExactInput && isHypercoreDeposit(request);
+
     const useExecute =
       supports7702 &&
       isRelayExecuteEnabled(messenger) &&
@@ -338,7 +344,7 @@ async function getSingleQuote(
         : {}),
       recipient: effectiveRequest.recipient ?? from,
       slippageTolerance,
-      tradeType: useExactInput ? 'EXACT_INPUT' : 'EXPECTED_OUTPUT',
+      tradeType: getTradeType(useExactInput, useExactOutput),
       user: from,
     };
 
@@ -613,6 +619,42 @@ async function processMoneyAccountPostQuote(
  * Hyperliquid-specific rewrites on transaction type.
  * @returns Normalized request.
  */
+/**
+ * Whether the quote deposits into HyperCore USDC.
+ *
+ * `normalizeRequest` remaps Arbitrum-USDC perps deposits to HyperCore before
+ * the quote is built, so the check is against the normalized target.
+ *
+ * @param request - Normalized quote request.
+ * @returns True when the target is HyperCore USDC.
+ */
+function isHypercoreDeposit(request: QuoteRequest): boolean {
+  return (
+    !request.isHyperliquidSource &&
+    request.targetChainId === CHAIN_ID_HYPERCORE &&
+    request.targetTokenAddress.toLowerCase() ===
+      HYPERCORE_USDC_ADDRESS.toLowerCase()
+  );
+}
+
+/**
+ * Resolve the Relay trade type for a quote.
+ *
+ * @param useExactInput - Whether the user specified the amount to send.
+ * @param useExactOutput - Whether the delivered amount must be guaranteed.
+ * @returns The Relay trade type.
+ */
+function getTradeType(
+  useExactInput: boolean | undefined,
+  useExactOutput: boolean,
+): RelayQuoteRequest['tradeType'] {
+  if (useExactInput) {
+    return 'EXACT_INPUT';
+  }
+
+  return useExactOutput ? 'EXACT_OUTPUT' : 'EXPECTED_OUTPUT';
+}
+
 function normalizeRequest(
   request: QuoteRequest,
   transaction: TransactionMeta,