diff --git a/http/src/main/java/io/micronaut/http/simple/SimpleHttpRequest.java b/http/src/main/java/io/micronaut/http/simple/SimpleHttpRequest.java
index 94b75c59d2..17e9709440 100644
--- a/http/src/main/java/io/micronaut/http/simple/SimpleHttpRequest.java
+++ b/http/src/main/java/io/micronaut/http/simple/SimpleHttpRequest.java
@@ -77,8 +77,17 @@ public MutableHttpRequest<B> cookie(Cookie cookie) {
 
     private void updateCookies() {
         headers.remove(HttpHeaders.COOKIE);
+        StringBuilder sb = new StringBuilder();
+        int count = 0;
         for (Cookie cookie : cookies.getAll()) {
-            headers.add(HttpHeaders.COOKIE, ClientCookieEncoder.INSTANCE.encode(cookie));
+            if (count > 0) {
+                sb.append("; ");
+            }
+            sb.append(ClientCookieEncoder.INSTANCE.encode(cookie));
+            count++;
+        }
+        if (sb.length() > 0) {
+            headers.set(HttpHeaders.COOKIE, sb.toString());
         }
     }
 
diff --git a/http/src/test/java/io/micronaut/http/cookie/CookieHeaderSingleValueTest.java b/http/src/test/java/io/micronaut/http/cookie/CookieHeaderSingleValueTest.java
new file mode 100644
index 0000000000..a26518ae54
--- /dev/null
+++ b/http/src/test/java/io/micronaut/http/cookie/CookieHeaderSingleValueTest.java
@@ -0,0 +1,93 @@
+package io.micronaut.http.cookie;
+
+import io.micronaut.http.HttpHeaders;
+import io.micronaut.http.MutableHttpRequest;
+import io.micronaut.http.cookie.Cookie;
+import io.micronaut.http.client.netty.NettyClientHttpRequestFactory;
+import io.micronaut.http.simple.SimpleHttpRequestFactory;
+import org.junit.jupiter.api.Test;
+
+import java.util.ArrayList;
+import java.util.LinkedHashSet;
+import java.util.List;
+import java.util.Set;
+import java.util.stream.Collectors;
+import java.util.stream.StreamSupport;
+
+import static org.junit.jupiter.api.Assertions.assertEquals;
+
+public class CookieHeaderSingleValueTest {
+
+    private static final Set<Cookie> COOKIES = new LinkedHashSet<Cookie>() {{
+        add(Cookie.of("a", "1"));
+        add(Cookie.of("b", "2"));
+        add(Cookie.of("a", "3"));
+    }};
+
+    private static String normalize(String header) {
+        if (header == null) {
+            return "";
+        }
+        // remove all whitespace for deterministic comparison (some implementations include a space after semicolon)
+        return header.replaceAll("\\s+", "").trim();
+    }
+
+    private static List<String> headerValues(MutableHttpRequest<?> request, String name) {
+        Iterable<String> it = request.getHeaders().getAll(name);
+        return StreamSupport.stream(it.spliterator(), false).collect(Collectors.toList());
+    }
+
+    @Test
+    public void simpleRequestAddsCookiesIntoSingleHeader() {
+        MutableHttpRequest<?> request = new SimpleHttpRequestFactory().get("/");
+        // ensure starting clean
+        request.getHeaders().remove(HttpHeaders.COOKIE);
+
+        for (Cookie c : COOKIES) {
+            request.cookie(c);
+        }
+
+        List<String> all = headerValues(request, HttpHeaders.COOKIE);
+        assertEquals(1, all.size(), "Expected exactly one Cookie header value for SimpleHttpRequest");
+
+        String header = request.getHeaders().get(HttpHeaders.COOKIE);
+        assertEquals("a=3;b=2", normalize(header));
+    }
+
+    @Test
+    public void nettyClientRequestAddsCookiesIntoSingleHeader() {
+        MutableHttpRequest<?> request = new NettyClientHttpRequestFactory().get("/");
+        // ensure starting clean
+        request.getHeaders().remove(HttpHeaders.COOKIE);
+
+        for (Cookie c : COOKIES) {
+            request.cookie(c);
+        }
+
+        List<String> all = headerValues(request, HttpHeaders.COOKIE);
+        assertEquals(1, all.size(), "Expected exactly one Cookie header value for NettyClientHttpRequest");
+
+        String header = request.getHeaders().get(HttpHeaders.COOKIE);
+        assertEquals("a=3;b=2", normalize(header));
+    }
+
+    @Test
+    public void addingCookiesTwiceKeepsSingleHeaderWithLastValueWin() {
+        MutableHttpRequest<?> request = new SimpleHttpRequestFactory().get("/");
+        request.getHeaders().remove(HttpHeaders.COOKIE);
+
+        for (Cookie c : COOKIES) {
+            request.cookie(c);
+        }
+        // add again to exercise mutation
+        for (Cookie c : COOKIES) {
+            request.cookie(c);
+        }
+
+        List<String> all = headerValues(request, HttpHeaders.COOKIE);
+        assertEquals(1, all.size(), "Expected exactly one Cookie header value after repeated additions");
+
+        String header = request.getHeaders().get(HttpHeaders.COOKIE);
+        assertEquals("a=3;b=2", normalize(header));
+    }
+}