diff --git a/cypress/helpers/index.js b/cypress/helpers/index.js
index e8f11a9251f..4c37fb32e38 100644
--- a/cypress/helpers/index.js
+++ b/cypress/helpers/index.js
@@ -98,3 +98,20 @@ const deleteGrant = (id) =>
     "DELETE",
     Cypress.env("admin_url") + "/trust/grants/jwt-bearer/issuers/" + id,
   )
+
+export const validateJwt = (jwt) =>
+  cy
+    .request({
+      method: "POST",
+      url: `${Cypress.env("client_url")}/oauth2/validate-jwt`,
+      form: true,
+      body: { jwt },
+    })
+    .then(({ body }) => body)
+
+export const rotateJwks = (set) =>
+  cy
+    .request("POST", `${Cypress.env("admin_url")}/keys/${set}`, {
+      alg: "RS256",
+    })
+    .then(({ body }) => body)
diff --git a/cypress/integration/oauth2/jwt.js b/cypress/integration/oauth2/jwt.js
index 8b9d0fe78f8..5057d78f376 100644
--- a/cypress/integration/oauth2/jwt.js
+++ b/cypress/integration/oauth2/jwt.js
@@ -1,7 +1,7 @@
 // Copyright © 2022 Ory Corp
 // SPDX-License-Identifier: Apache-2.0
 
-import { createClient, prng } from "../../helpers"
+import { createClient, prng, validateJwt } from "../../helpers"
 
 const accessTokenStrategies = ["opaque", "jwt"]
 
@@ -44,15 +44,12 @@ describe("OAuth 2.0 JSON Web Token Access Tokens", () => {
               expect(token.refresh_token).to.not.be.empty
               expect(token.access_token.split(".").length).to.equal(3)
               expect(token.refresh_token.split(".").length).to.equal(2)
-            })
 
-          cy.request(`${Cypress.env("client_url")}/oauth2/validate-jwt`)
-            .its("body")
-            .then((body) => {
-              console.log(body)
-              expect(body.sub).to.eq("foo@bar.com")
-              expect(body.client_id).to.eq(client.client_id)
-              expect(body.jti).to.not.be.empty
+              validateJwt(token.access_token).then(({ payload }) => {
+                expect(payload.sub).to.eq("foo@bar.com")
+                expect(payload.client_id).to.eq(client.client_id)
+                expect(payload.jti).to.not.be.empty
+              })
             })
         })
       })
diff --git a/cypress/integration/oauth2/refresh_token.js b/cypress/integration/oauth2/refresh_token.js
index 2ddf7d30f19..dcd9cacbf19 100644
--- a/cypress/integration/oauth2/refresh_token.js
+++ b/cypress/integration/oauth2/refresh_token.js
@@ -1,7 +1,7 @@
 // Copyright © 2022 Ory Corp
 // SPDX-License-Identifier: Apache-2.0
 
-import { createClient, prng } from "../../helpers"
+import { createClient, prng, rotateJwks, validateJwt } from "../../helpers"
 
 const accessTokenStrategies = ["opaque", "jwt"]
 
@@ -100,6 +100,61 @@ describe("The OAuth 2.0 Refresh Token Grant", function () {
           })
         })
       })
+
+      const validateJwtAndGetKid = (token) =>
+        validateJwt(token).then(({ header }) => header.kid)
+
+      it("should refresh the Access and ID Token with newly rotated keys", function () {
+        if (
+          accessTokenStrategy === "opaque" ||
+          (Cypress.env("jwt_enabled") !== "true" &&
+            !Boolean(Cypress.env("jwt_enabled")))
+        ) {
+          this.skip()
+        }
+
+        const referrer = `${Cypress.env("client_url")}/empty`
+        cy.visit(referrer, {
+          failOnStatusCode: false,
+        })
+
+        createClient({
+          scope: "offline_access openid",
+          redirect_uris: [referrer],
+          grant_types: ["authorization_code", "refresh_token"],
+          response_types: ["code"],
+          token_endpoint_auth_method: "none",
+        }).then((client) => {
+          cy.authCodeFlowBrowser(client, {
+            consent: {
+              scope: ["offline_access", "openid"],
+            },
+            createClient: false,
+          }).then(({ body: tokensBefore }) => {
+            const kidsBefore = {
+              accessToken: validateJwtAndGetKid(tokensBefore.access_token),
+              idToken: validateJwtAndGetKid(tokensBefore.id_token),
+            }
+
+            rotateJwks("hydra.jwt.access-token")
+            rotateJwks("hydra.openid.id-token")
+
+            cy.refreshTokenBrowser(client, tokensBefore.refresh_token).then(
+              ({ body: tokensAfter }) => {
+                const kidsAfter = {
+                  accessToken: validateJwtAndGetKid(tokensAfter.access_token),
+                  idToken: validateJwtAndGetKid(tokensAfter.id_token),
+                }
+
+                expect(kidsAfter.accessToken).to.not.equal(
+                  kidsBefore.accessToken,
+                )
+                expect(kidsAfter.idToken).to.not.equal(kidsBefore.idToken)
+              },
+            )
+          })
+        })
+      })
     })
   })
 })
diff --git a/cypress/support/commands.js b/cypress/support/commands.js
index 2f75293404d..3c2d610e1e5 100644
--- a/cypress/support/commands.js
+++ b/cypress/support/commands.js
@@ -196,10 +196,9 @@ Cypress.Commands.add(
       })
     }
     if (doCreateClient) {
-      createClient(client).then(run)
-      return
+      return createClient(client).then(run)
     }
-    run(client)
+    return run(client)
   },
 )
 
diff --git a/oauth2/handler.go b/oauth2/handler.go
index 3f1a633038d..0a4ea1564ea 100644
--- a/oauth2/handler.go
+++ b/oauth2/handler.go
@@ -1021,6 +1021,32 @@ func (h *Handler) oauth2TokenExchange(w http.ResponseWriter, r *http.Request) {
 		}
 	}
 
+	if accessRequest.GetGrantTypes().ExactOne(string(fosite.GrantTypeRefreshToken)) {
+		var accessTokenKeyID string
+		if h.c.AccessTokenStrategy(ctx, client.AccessTokenStrategySource(accessRequest.GetClient())) == "jwt" {
+			accessTokenKeyID, err = h.r.AccessTokenJWTStrategy().GetPublicKeyID(ctx)
+			if err != nil {
+				h.logOrAudit(err, r)
+				h.r.OAuth2Provider().WriteAccessError(ctx, w, accessRequest, err)
+				events.Trace(ctx, events.TokenExchangeError, events.WithRequest(accessRequest))
+				return
+			}
+		}
+
+		openIDKeyID, err := h.r.OpenIDJWTStrategy().GetPublicKeyID(ctx)
+		if err != nil {
+			h.logOrAudit(err, r)
+			h.r.OAuth2Provider().WriteAccessError(ctx, w, accessRequest, err)
+			events.Trace(ctx, events.TokenExchangeError, events.WithRequest(accessRequest))
+			return
+		}
+
+		if sess, ok := accessRequest.GetSession().(*Session); ok {
+			sess.KID = accessTokenKeyID
+			sess.DefaultSession.Headers.Add("kid", openIDKeyID)
+		}
+	}
+
 	for _, hook := range h.r.AccessRequestHooks() {
 		if err = hook(ctx, accessRequest); err != nil {
 			h.logOrAudit(err, r)
diff --git a/test/e2e/oauth2-client/src/index.js b/test/e2e/oauth2-client/src/index.js
index b27512bedeb..7a211a758ab 100644
--- a/test/e2e/oauth2-client/src/index.js
+++ b/test/e2e/oauth2-client/src/index.js
@@ -179,23 +179,24 @@ app.get("/oauth2/revoke", (req, res) => {
     })
 })
 
-app.get("/oauth2/validate-jwt", (req, res) => {
+app.post("/oauth2/validate-jwt", (req, res) => {
   const client = jwksClient({
     jwksUri: new URL("/.well-known/jwks.json", config.public).toString(),
   })
 
   jwt.verify(
-    req.session.oauth2_flow.token.access_token,
+    req.body.jwt,
     (header, callback) => {
       client.getSigningKey(header.kid, function (err, key) {
         const signingKey = key.publicKey || key.rsaPublicKey
         callback(null, signingKey)
       })
     },
+    { complete: true },
     (err, decoded) => {
       if (err) {
         console.error(err)
-        res.send(400)
+        res.status(400).send(JSON.stringify({ error: err.toString() }))
         return
       }