diff --git a/index.js b/index.js
index 486c3bb..dddff40 100644
--- a/index.js
+++ b/index.js
@@ -121,11 +121,13 @@ function fastifyJwt (fastify, options, next) {
     secretOrPrivateKey = secretOrPublicKey = secret
   }
 
+  let hasStaticPrivateKey = false
   let hasStaticPublicKey = false
   let secretCallbackSign = secretOrPrivateKey
   let secretCallbackVerify = secretOrPublicKey
   if (typeof secretCallbackSign !== 'function') {
     secretCallbackSign = wrapStaticSecretInCallback(secretCallbackSign)
+    hasStaticPrivateKey = true
   }
   if (typeof secretCallbackVerify !== 'function') {
     secretCallbackVerify = wrapStaticSecretInCallback(secretCallbackVerify)
@@ -289,9 +291,11 @@ function fastifyJwt (fastify, options, next) {
     return token
   }
 
-  function mergeOptionsWithKey (options, useProvidedPrivateKey) {
+  function mergeOptionsWithKey (options, useProvidedPrivateKey, preferOptionsKey) {
     if (useProvidedPrivateKey && (typeof useProvidedPrivateKey !== 'boolean')) {
-      return Object.assign({}, options, { key: options.key ?? useProvidedPrivateKey })
+      return preferOptionsKey && options.key
+        ? Object.assign({ key: useProvidedPrivateKey }, options)
+        : Object.assign({}, options, { key: useProvidedPrivateKey })
     } else {
       const key = useProvidedPrivateKey ? secretOrPrivateKey : secretOrPublicKey
       return Object.assign(!options.key ? { key } : {}, options)
@@ -409,7 +413,8 @@ function fastifyJwt (fastify, options, next) {
       },
       function sign (secretOrPrivateKey, callback) {
         if (useLocalSigner) {
-          const signerOptions = mergeOptionsWithKey(options.sign || options, secretOrPrivateKey)
+          const localSignOptions = options.sign || options
+          const signerOptions = mergeOptionsWithKey(localSignOptions, secretOrPrivateKey, hasStaticPrivateKey)
           const localSigner = createSigner(signerOptions)
           const token = localSigner(payload)
           callback(null, token)
@@ -467,7 +472,6 @@ function fastifyJwt (fastify, options, next) {
     }
 
     const useGlobalOptions = !options
-
     if (typeof options === 'function') {
       next = options
       options = {}
@@ -508,7 +512,8 @@ function fastifyJwt (fastify, options, next) {
       },
       function verify (secretOrPublicKey, callback) {
         try {
-          const verifierOptions = mergeOptionsWithKey(options.verify || options, secretOrPublicKey)
+          const localVerifyOptions = options.verify || options
+          const verifierOptions = mergeOptionsWithKey(localVerifyOptions, secretOrPublicKey, hasStaticPublicKey)
           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 fa79532..b8229f2 100644
--- a/test/jwt.test.js
+++ b/test/jwt.test.js
@@ -2,7 +2,7 @@
 
 const { test } = require('node:test')
 const Fastify = require('fastify')
-const { createSigner } = require('fast-jwt')
+const { createSigner, createVerifier } = require('fast-jwt')
 const jwt = require('..')
 const defaultExport = require('..').default
 const { fastifyJwt: namedExport } = require('..')
@@ -3133,3 +3133,52 @@ test('local sign options should not overwrite global sign options', async functi
 
   t.assert.strictEqual(fastify.jwt.options.sign.expiresIn, '15m')
 })
+
+test('reply.jwtSign should honor a per-request sign.key override', async function (t) {
+  t.plan(2)
+
+  const fastify = Fastify()
+  fastify.register(jwt, { secret: 'hunter2' })
+
+  fastify.post('/sign', async function (request, reply) {
+    return reply.jwtSign(request.body, { sign: { key: 'override' } })
+  })
+
+  await fastify.ready()
+
+  const response = await fastify.inject({
+    method: 'post',
+    url: '/sign',
+    payload: { foo: 'bar' }
+  })
+
+  t.assert.strictEqual(response.statusCode, 200)
+
+  const decoded = createVerifier({ key: 'override' })(response.payload)
+  t.assert.strictEqual(decoded.foo, 'bar')
+})
+
+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')
+})