diff --git a/http-core/src/main/scala/org/apache/pekko/http/impl/engine/http2/Http2.scala b/http-core/src/main/scala/org/apache/pekko/http/impl/engine/http2/Http2.scala
index 2cdb6a42c4..eaac91b913 100644
--- a/http-core/src/main/scala/org/apache/pekko/http/impl/engine/http2/Http2.scala
+++ b/http-core/src/main/scala/org/apache/pekko/http/impl/engine/http2/Http2.scala
@@ -90,11 +90,15 @@ private[http] final class Http2Ext(implicit val system: ActorSystem)
       else if (connectionContext.isSecure) settings.defaultHttpsPort
       else settings.defaultHttpPort
 
+    val handlerWithErrorHandling = withErrorHandling(log, handler)
+
     val http1: HttpImplementation =
-      Flow[HttpRequest].mapAsync(settings.pipeliningLimit)(handleUpgradeRequests(handler, settings, log))
+      Flow[HttpRequest].mapAsync(settings.pipeliningLimit)(handleUpgradeRequests(handler, handlerWithErrorHandling,
+        settings, log))
         .joinMat(GracefulTerminatorStage(system, settings).atop(http.serverLayer(settings, log = log)))(Keep.right)
     val http2: HttpImplementation =
-      Http2Blueprint.handleWithStreamIdHeader(settings.http2Settings.maxConcurrentStreams)(handler)(system.dispatcher)
+      Http2Blueprint.handleWithStreamIdHeader(settings.http2Settings.maxConcurrentStreams)(handlerWithErrorHandling)(
+        system.dispatcher)
         .joinMat(Http2Blueprint.serverStackTls(settings, log, telemetry, Http().dateHeaderRendering))(Keep.right)
 
     val masterTerminator = new MasterServerTerminator(log)
@@ -138,6 +142,23 @@ private[http] final class Http2Ext(implicit val system: ActorSystem)
       }.to(Sink.ignore).run()
   }
 
+  private def withErrorHandling(
+      log: LoggingAdapter,
+      handler: HttpRequest => Future[HttpResponse]): HttpRequest => Future[HttpResponse] = { request =>
+    try {
+      handler(request).recover {
+        case NonFatal(ex) => handleHandlerError(log, ex)
+      }(ExecutionContext.parasitic)
+    } catch {
+      case NonFatal(ex) => Future.successful(handleHandlerError(log, ex))
+    }
+  }
+
+  private def handleHandlerError(log: LoggingAdapter, ex: Throwable): HttpResponse = {
+    log.error(ex, "Internal server error, sending 500 response")
+    HttpResponse(StatusCodes.InternalServerError)
+  }
+
   private def prepareServerAttributes(settings: ServerSettings, incoming: Tcp.IncomingConnection) = {
     val attrs = Http.prepareAttributes(settings, incoming)
     if (telemetry == NoOpTelemetry) attrs
@@ -149,6 +170,7 @@ private[http] final class Http2Ext(implicit val system: ActorSystem)
 
   private def handleUpgradeRequests(
       handler: HttpRequest => Future[HttpResponse],
+      handlerWithErrorHandling: HttpRequest => Future[HttpResponse],
       settings: ServerSettings,
       log: LoggingAdapter): HttpRequest => Future[HttpResponse] = { req =>
     req.header[Upgrade] match {
@@ -172,8 +194,8 @@ private[http] final class Http2Ext(implicit val system: ActorSystem)
               Flow[HttpRequest]
                 .watchTermination(Keep.right)
                 .prepend(injectedRequest)
-                .via(Http2Blueprint.handleWithStreamIdHeader(settings.http2Settings.maxConcurrentStreams)(handler)(
-                  system.dispatcher))
+                .via(Http2Blueprint.handleWithStreamIdHeader(settings.http2Settings.maxConcurrentStreams)(
+                  handlerWithErrorHandling)(system.dispatcher))
                 // the settings from the header are injected into the blueprint as initial demuxer settings
                 .joinMat(Http2Blueprint.serverStack(settings, log, settingsFromHeader, true, telemetry,
                   Http().dateHeaderRendering))(Keep.left))
diff --git a/http-core/src/main/scala/org/apache/pekko/http/impl/engine/http2/RequestParsing.scala b/http-core/src/main/scala/org/apache/pekko/http/impl/engine/http2/RequestParsing.scala
index 8b3f148b7c..99e0c20be9 100644
--- a/http-core/src/main/scala/org/apache/pekko/http/impl/engine/http2/RequestParsing.scala
+++ b/http-core/src/main/scala/org/apache/pekko/http/impl/engine/http2/RequestParsing.scala
@@ -160,6 +160,9 @@ private[http2] object RequestParsing {
             case ":status" =>
               protocolError("Pseudo-header ':status' is for responses only; it cannot appear in a request")
 
+            case name if name.startsWith(":") =>
+              protocolError(s"Unexpected pseudo-header '$name' in request")
+
             case "content-length" =>
               if (contentLength == -1) {
                 val contentLengthValue = ContentLength.get(value).toLong
diff --git a/http2-tests/src/test/scala/org/apache/pekko/http/impl/engine/http2/Http2ClientServerSpec.scala b/http2-tests/src/test/scala/org/apache/pekko/http/impl/engine/http2/Http2ClientServerSpec.scala
index 96ddec9f66..6f718ec56a 100644
--- a/http2-tests/src/test/scala/org/apache/pekko/http/impl/engine/http2/Http2ClientServerSpec.scala
+++ b/http2-tests/src/test/scala/org/apache/pekko/http/impl/engine/http2/Http2ClientServerSpec.scala
@@ -30,7 +30,6 @@ import pekko.http.scaladsl.model.{
   HttpHeader,
   HttpMethod,
   HttpMethods,
-  HttpProtocols,
   HttpRequest,
   HttpResponse,
   RequestResponseAssociation,
@@ -45,6 +44,8 @@ import pekko.http.scaladsl.unmarshalling.Unmarshal
 import pekko.stream.StreamTcpException
 import pekko.stream.scaladsl.{ Sink, Source }
 import pekko.stream.testkit.{ TestPublisher, TestSubscriber }
+import pekko.stream.testkit.Utils.TE
+import pekko.testkit.EventFilter
 import pekko.testkit.TestProbe
 import pekko.util.ByteString
 
@@ -144,6 +145,31 @@ class Http2ClientServerSpec extends PekkoSpecWithMaterializer(
       val response = expectClientResponse()
       response.status should be(StatusCodes.BadRequest)
     }
+
+    "return internal server error when handler future fails" in new TestSetup {
+      sendClientRequest()
+      val serverRequest = expectServerRequest()
+
+      EventFilter[TE](message = "boom", occurrences = 1).intercept {
+        serverRequest.promise.failure(TE("boom"))
+        val response = expectClientResponse()
+        response.status should be(StatusCodes.InternalServerError)
+      }
+
+      sendClientRequest()
+      val nextServerRequest = expectServerRequest()
+      nextServerRequest.sendResponse(HttpResponse())
+      expectClientResponse().status should be(StatusCodes.OK)
+    }
+
+    "return internal server error when handler throws synchronously" in new TestSetup {
+      override def handler: HttpRequest => Future[HttpResponse] = _ => throw TE("boom-sync")
+
+      EventFilter[TE](message = "boom-sync", occurrences = 1).intercept {
+        sendClientRequest()
+        expectClientResponse().status should be(StatusCodes.InternalServerError)
+      }
+    }
   }
 
   case class ServerRequest(request: HttpRequest, promise: Promise[HttpResponse]) {
@@ -169,7 +195,7 @@ class Http2ClientServerSpec extends PekkoSpecWithMaterializer(
     def serverSettings: ServerSettings = ServerSettings(system)
     def clientSettings: ClientConnectionSettings = ClientConnectionSettings(system)
     private lazy val serverRequestProbe = TestProbe()
-    private lazy val handler: HttpRequest => Future[HttpResponse] = { req =>
+    def handler: HttpRequest => Future[HttpResponse] = { req =>
       val p = Promise[HttpResponse]()
       serverRequestProbe.ref ! ServerRequest(req, p)
       p.future