diff --git a/lib/helpers/validate_dpop.js b/lib/helpers/validate_dpop.js
index e3a6267ce..dc753140a 100644
--- a/lib/helpers/validate_dpop.js
+++ b/lib/helpers/validate_dpop.js
@@ -40,10 +40,7 @@ export default async (ctx, accessToken) => {
   if (typeof requireNonce !== 'boolean') {
     throw new Error('features.dPoP.requireNonce must return a boolean');
   }
-
-  if (DPoPNonces) {
-    ctx.set('DPoP-Nonce', DPoPNonces.nextNonce());
-  } else if (requireNonce) {
+  if (requireNonce && !DPoPNonces) {
     throw new Error('features.dPoP.nonceSecret configuration is missing');
   }
 
@@ -70,6 +67,8 @@ export default async (ctx, accessToken) => {
       if (diff > DPOP_OK_WINDOW) {
         throw new InvalidDpopProof('DPoP proof iat is not recent enough');
       }
+    } else if (!DPoPNonces) {
+      throw new InvalidDpopProof('DPoP nonces are not supported');
     }
 
     if (payload.htm !== ctx.method) {
@@ -103,14 +102,21 @@ export default async (ctx, accessToken) => {
     throw new InvalidDpopProof('invalid DPoP key binding', err.message);
   }
 
+  const nextNonce = DPoPNonces?.nextNonce();
   if (!payload.nonce && requireNonce) {
+    ctx.set('DPoP-Nonce', nextNonce);
     throw new UseDpopNonce('nonce is required in the DPoP proof');
   }
 
-  if (payload.nonce && (!DPoPNonces || !DPoPNonces.checkNonce(payload.nonce))) {
+  if (payload.nonce && !DPoPNonces.checkNonce(payload.nonce)) {
+    ctx.set('DPoP-Nonce', nextNonce);
     throw new UseDpopNonce('invalid nonce in DPoP proof');
   }
 
+  if (payload.nonce !== nextNonce) {
+    ctx.set('DPoP-Nonce', nextNonce);
+  }
+
   const thumbprint = await calculateJwkThumbprint(protectedHeader.jwk);
 
   const result = { thumbprint, jti: payload.jti, iat: payload.iat };
diff --git a/test/dpop/dpop.test.js b/test/dpop/dpop.test.js
index 00833662f..cbeece648 100644
--- a/test/dpop/dpop.test.js
+++ b/test/dpop/dpop.test.js
@@ -994,7 +994,11 @@ describe('features.dPoP', () => {
         })
         .set('DPoP', await DPoP(this.keypair, `${this.provider.issuer}${this.suitePath('/request')}`, 'POST', nonce))
         .type('form')
-        .expect(201);
+        .expect(201)
+        .expect((response) => {
+          // because the sent one is fresh
+          expect(response.headers).not.to.have.property('dpop-nonce');
+        });
     });
 
     it('@ userinfo', async function () {
@@ -1012,6 +1016,10 @@ describe('features.dPoP', () => {
         .send({ grant_type: 'client_credentials' })
         .set('DPoP', await DPoP(this.keypair, `${this.provider.issuer}${this.suitePath('/me')}`, 'GET', nonce, 'foo'))
         .expect(401)
+        .expect((response) => {
+          // because the sent one is fresh
+          expect(response.headers).not.to.have.property('dpop-nonce');
+        })
         .expect({ error: 'invalid_token', error_description: 'invalid token provided' });
     });
 
@@ -1031,7 +1039,11 @@ describe('features.dPoP', () => {
         .send({ grant_type: 'client_credentials' })
         .set('DPoP', await DPoP(this.keypair, `${this.provider.issuer}${this.suitePath('/token')}`, 'POST', nonce))
         .type('form')
-        .expect(200);
+        .expect(200)
+        .expect((response) => {
+          // because the sent one is fresh
+          expect(response.headers).not.to.have.property('dpop-nonce');
+        });
     });
   });
 });