diff --git a/core/src/main/scala/org/http4s/Message.scala b/core/src/main/scala/org/http4s/Message.scala
index 418dd33177b..c75b4910aab 100644
--- a/core/src/main/scala/org/http4s/Message.scala
+++ b/core/src/main/scala/org/http4s/Message.scala
@@ -340,7 +340,14 @@ sealed abstract case class Request[F[_]](
 
   /** Add a Cookie header for the provided [[Cookie]] */
   def addCookie(cookie: RequestCookie): Self =
-    putHeaders(Cookie(NonEmptyList.of(cookie)))
+    headers
+      .get(Cookie)
+      .fold(putHeaders(Cookie(NonEmptyList.of(cookie)))) { preExistingCookie =>
+        removeHeader(Cookie).putHeaders(
+          Header(
+            Cookie.name.value,
+            s"${preExistingCookie.value}; ${cookie.name}=${cookie.content}"))
+      }
 
   /** Add a Cookie header with the provided values */
   def addCookie(name: String, content: String): Self =
diff --git a/tests/src/test/scala/org/http4s/MessageSpec.scala b/tests/src/test/scala/org/http4s/MessageSpec.scala
index 859782674df..0ec53c4e12d 100644
--- a/tests/src/test/scala/org/http4s/MessageSpec.scala
+++ b/tests/src/test/scala/org/http4s/MessageSpec.scala
@@ -67,6 +67,15 @@ class MessageSpec extends Http4sSpec {
           .map(_.value) must beSome("token=value")
       }
 
+      "contain a single Cookie header when multiple explicit cookies are added" in {
+        Request(Method.GET)
+          .addCookie(RequestCookie("token1", "value1"))
+          .addCookie(RequestCookie("token2", "value2"))
+          .headers
+          .get("Cookie".ci)
+          .map(_.value) must beSome("token1=value1; token2=value2")
+      }
+
       "contain a Cookie header when a name/value pair is added" in {
         Request(Method.GET)
           .addCookie("token", "value")
@@ -74,6 +83,15 @@ class MessageSpec extends Http4sSpec {
           .get("Cookie".ci)
           .map(_.value) must beSome("token=value")
       }
+
+      "contain a single Cookie header when name/value pairs are added" in {
+        Request(Method.GET)
+          .addCookie("token1", "value1")
+          .addCookie("token2", "value2")
+          .headers
+          .get("Cookie".ci)
+          .map(_.value) must beSome("token1=value1; token2=value2")
+      }
     }
 
     "Request.with..." should {
@@ -118,7 +136,7 @@ class MessageSpec extends Http4sSpec {
       "redact Cookie Headers" in {
         val request =
           Request[IO](Method.GET).addCookie("token", "value").addCookie("token2", "value2")
-        request.toString must_== ("Request(method=GET, uri=/, headers=Headers(Cookie: <REDACTED>, Cookie: <REDACTED>))")
+        request.toString must_== ("Request(method=GET, uri=/, headers=Headers(Cookie: <REDACTED>))")
       }
     }
   }