diff --git a/extensions/csrf-reactive/runtime/src/main/java/io/quarkus/csrf/reactive/runtime/CsrfRequestResponseReactiveFilter.java b/extensions/csrf-reactive/runtime/src/main/java/io/quarkus/csrf/reactive/runtime/CsrfRequestResponseReactiveFilter.java
index 25df381ac7b59..f8f00b715f8a1 100644
--- a/extensions/csrf-reactive/runtime/src/main/java/io/quarkus/csrf/reactive/runtime/CsrfRequestResponseReactiveFilter.java
+++ b/extensions/csrf-reactive/runtime/src/main/java/io/quarkus/csrf/reactive/runtime/CsrfRequestResponseReactiveFilter.java
@@ -87,12 +87,26 @@ public void filter(ResteasyReactiveContainerRequestContext requestContext, Routi
         if (requestMethodIsSafe(requestContext)) {
             // safe HTTP method, tolerate the absence of a token
             if (isCsrfTokenRequired(routing, config)) {
-                // Set the CSRF cookie with a randomly generated value
-                byte[] tokenBytes = new byte[config.tokenSize];
-                secureRandom.nextBytes(tokenBytes);
-                routing.put(CSRF_TOKEN_BYTES_KEY, tokenBytes);
-                routing.put(CSRF_TOKEN_KEY, Base64.getUrlEncoder().withoutPadding().encodeToString(tokenBytes));
-
+                if (cookieToken == null) {
+                    generateNewCsrfToken(routing, config);
+                } else {
+                    String csrfTokenHeaderParam = requestContext.getHeaderString(config.tokenHeaderName);
+                    if (csrfTokenHeaderParam != null) {
+                        LOG.debugf("CSRF token found in the token header");
+                        // Verify the header, make sure the header value, possibly signed, is returned as the next cookie value
+                        verifyCsrfToken(requestContext, routing, config, cookieToken, csrfTokenHeaderParam);
+                    } else if (!config.tokenSignatureKey.isEmpty()) {
+                        // If the signature is required, then we can not use the current cookie value
+                        // as the HTML form token key because it represents a signed value of the previous key
+                        // and it will lead to the double-signing issue if this value is reused as the key.
+                        // It should be fine for simple HTML forms anyway
+                        generateNewCsrfToken(routing, config);
+                    } else {
+                        // Make sure the same cookie value is returned
+                        routing.put(CSRF_TOKEN_KEY, cookieToken);
+                        routing.put(CSRF_TOKEN_BYTES_KEY, Base64.getUrlDecoder().decode(cookieToken));
+                    }
+                }
                 routing.put(NEW_COOKIE_REQUIRED, true);
             }
         } else if (config.verifyToken) {
@@ -139,6 +153,14 @@ public void filter(ResteasyReactiveContainerRequestContext requestContext, Routi
         }
     }
 
+    private void generateNewCsrfToken(RoutingContext routing, CsrfReactiveConfig config) {
+        // Set the CSRF cookie with a randomly generated value
+        byte[] tokenBytes = new byte[config.tokenSize];
+        secureRandom.nextBytes(tokenBytes);
+        routing.put(CSRF_TOKEN_BYTES_KEY, tokenBytes);
+        routing.put(CSRF_TOKEN_KEY, Base64.getUrlEncoder().withoutPadding().encodeToString(tokenBytes));
+    }
+
     private void verifyCsrfToken(ResteasyReactiveContainerRequestContext requestContext, RoutingContext routing,
             CsrfReactiveConfig config, String cookieToken, String csrfToken) {
         if (cookieToken == null) {
@@ -160,6 +182,7 @@ private void verifyCsrfToken(ResteasyReactiveContainerRequestContext requestCont
                 return;
             } else {
                 routing.put(CSRF_TOKEN_KEY, csrfToken);
+                routing.put(CSRF_TOKEN_BYTES_KEY, Base64.getUrlDecoder().decode(csrfToken));
                 routing.put(CSRF_TOKEN_VERIFIED, true);
                 // reset the cookie
                 routing.put(NEW_COOKIE_REQUIRED, true);
diff --git a/integration-tests/csrf-reactive/src/test/java/io/quarkus/it/csrf/CsrfReactiveTest.java b/integration-tests/csrf-reactive/src/test/java/io/quarkus/it/csrf/CsrfReactiveTest.java
index a8a937e1906a8..e317f75c71eb3 100644
--- a/integration-tests/csrf-reactive/src/test/java/io/quarkus/it/csrf/CsrfReactiveTest.java
+++ b/integration-tests/csrf-reactive/src/test/java/io/quarkus/it/csrf/CsrfReactiveTest.java
@@ -4,6 +4,7 @@
 import static org.junit.jupiter.api.Assertions.assertEquals;
 import static org.junit.jupiter.api.Assertions.assertNotNull;
 import static org.junit.jupiter.api.Assertions.assertNull;
+import static org.junit.jupiter.api.Assertions.assertTrue;
 import static org.junit.jupiter.api.Assertions.fail;
 
 import java.net.URL;
@@ -56,6 +57,8 @@ public void testCsrfTokenInForm() throws Exception {
             assertNotNull(htmlPage.getWebResponse().getResponseHeaderValue("Set-Cookie"));
             assertEquals("alice:true:tokenHeaderIsSet=false", textPage.getContent());
 
+            Cookie cookie1 = webClient.getCookieManager().getCookie("csrftoken");
+
             // This request which returns String is not CSRF protected
             textPage = webClient.getPage("http://localhost:8081/service/hello");
             assertEquals("hello", textPage.getContent());
@@ -67,6 +70,11 @@ public void testCsrfTokenInForm() throws Exception {
             assertNotNull(htmlPage.getWebResponse().getResponseHeaderValue("Set-Cookie"));
             assertEquals("alice:true:tokenHeaderIsSet=false", textPage.getContent());
 
+            Cookie cookie2 = webClient.getCookieManager().getCookie("csrftoken");
+
+            assertEquals(cookie1.getValue(), cookie2.getValue());
+            assertTrue(cookie1.getExpires().before(cookie2.getExpires()));
+
             webClient.getCookieManager().clearCookies();
         }
     }
@@ -366,6 +374,12 @@ private void assurePostFormPath(io.vertx.ext.web.client.WebClient vertxWebClient
         if (responseBody != null) {
             assertEquals(responseBody, result.result().bodyAsString(), path);
         }
+        if (expectedStatus != 400) {
+            String[] nextCookie = result.result().cookies().get(0).split(";");
+            String[] cookieNameValue = nextCookie[0].trim().split("=");
+            assertEquals(csrfCookie.getName(), cookieNameValue[0]);
+            assertEquals(csrfCookie.getValue(), cookieNameValue[1]);
+        }
     }
 
     private void assurePostJsonPath(io.vertx.ext.web.client.WebClient vertxWebClient, String path,