diff --git a/index.js b/index.js
index 3b7c973..32b8f1f 100644
--- a/index.js
+++ b/index.js
@@ -383,6 +383,10 @@ function fastifyJwt (fastify, options, next) {
       })
     }
 
+    // Capture any per-request `key` before merging, so it can take precedence
+    // over the resolved secret (as documented for the `sign.key` option).
+    const requestSignKey = options.sign ? options.sign.key : options.key
+
     if (options.sign) {
       const localSignOptions = convertTemporalProps(options.sign)
       // New supported contract, options supports sign and can expand
@@ -409,7 +413,11 @@ function fastifyJwt (fastify, options, next) {
       },
       function sign (secretOrPrivateKey, callback) {
         if (useLocalSigner) {
-          const signerOptions = mergeOptionsWithKey(options.sign || options, secretOrPrivateKey)
+          const localSignOptions = options.sign || options
+          // A per-request `key` overrides the resolved secret; otherwise the resolved secret is used.
+          const signerOptions = requestSignKey
+            ? localSignOptions
+            : mergeOptionsWithKey(localSignOptions, secretOrPrivateKey)
           const localSigner = createSigner(signerOptions)
           const token = localSigner(payload)
           callback(null, token)
@@ -477,6 +485,10 @@ function fastifyJwt (fastify, options, next) {
       options = {}
     }
 
+    // Capture any per-request `key` before merging, so it can take precedence
+    // over the resolved secret (as documented for the `verify.key` option).
+    const requestVerifyKey = options.verify ? options.verify.key : options.key
+
     if (options.decode || options.verify) {
       const localVerifyOptions = convertTemporalProps(options.verify, true)
       // New supported contract, options supports both decode and verify
@@ -508,7 +520,11 @@ function fastifyJwt (fastify, options, next) {
       },
       function verify (secretOrPublicKey, callback) {
         try {
-          const verifierOptions = mergeOptionsWithKey(options.verify || options, secretOrPublicKey)
+          const localVerifyOptions = options.verify || options
+          // A per-request `key` overrides the resolved secret; otherwise the resolved secret is used.
+          const verifierOptions = requestVerifyKey
+            ? localVerifyOptions
+            : mergeOptionsWithKey(localVerifyOptions, secretOrPublicKey)
           const localVerifier = getVerifier(verifierOptions, useGlobalOptions)
           const verifyResult = localVerifier(token)
           if (verifyResult && typeof verifyResult.then === 'function') {
diff --git a/test/jwt.test.js b/test/jwt.test.js
index c9a6823..1f6842b 100644
--- a/test/jwt.test.js
+++ b/test/jwt.test.js
@@ -3036,3 +3036,28 @@ test('local sign options should not overwrite global sign options', async functi
 
   t.assert.strictEqual(fastify.jwt.options.sign.expiresIn, '15m')
 })
+
+test('request.jwtVerify should honor a per-request verify.key override', async function (t) {
+  t.plan(2)
+
+  const fastify = Fastify()
+  fastify.register(jwt, { secret: 'hunter2' })
+
+  fastify.get('/verify', async function (request) {
+    return request.jwtVerify({ verify: { key: 'override' } })
+  })
+
+  await fastify.ready()
+
+  // Token signed with the override key, not the registration secret.
+  const token = createSigner({ key: 'override' })({ foo: 'bar' })
+
+  const response = await fastify.inject({
+    method: 'get',
+    url: '/verify',
+    headers: { authorization: `Bearer ${token}` }
+  })
+
+  t.assert.strictEqual(response.statusCode, 200)
+  t.assert.strictEqual(JSON.parse(response.payload).foo, 'bar')
+})