diff --git a/Justfile b/Justfile
index 25a739b602..d7ff4a3e63 100644
--- a/Justfile
+++ b/Justfile
@@ -114,7 +114,7 @@ integration-tests *test:
   #!/bin/bash
   set -euo pipefail
   testName=${1:-}
-  go test -fullpath -count 1 -v -tags integration -run "$testName" ./...
+  go test -fullpath -count 1 -v -tags integration -run "$testName" -p 1 ./...
 
 # Run README doc tests
 test-readme *args:
diff --git a/backend/controller/controller.go b/backend/controller/controller.go
index b379d75cf0..46e96487c3 100644
--- a/backend/controller/controller.go
+++ b/backend/controller/controller.go
@@ -26,6 +26,7 @@ import (
 	"github.com/jellydator/ttlcache/v3"
 	"github.com/jpillora/backoff"
 	"golang.org/x/exp/maps"
+	"golang.org/x/sync/errgroup"
 	"google.golang.org/protobuf/proto"
 	"google.golang.org/protobuf/types/known/structpb"
 	"google.golang.org/protobuf/types/known/timestamppb"
@@ -45,6 +46,7 @@ import (
 	cf "github.com/TBD54566975/ftl/common/configuration"
 	frontend "github.com/TBD54566975/ftl/frontend"
 	"github.com/TBD54566975/ftl/internal/cors"
+	ftlhttp "github.com/TBD54566975/ftl/internal/http"
 	"github.com/TBD54566975/ftl/internal/log"
 	ftlmaps "github.com/TBD54566975/ftl/internal/maps"
 	"github.com/TBD54566975/ftl/internal/model"
@@ -67,6 +69,7 @@ type CommonConfig struct {
 
 type Config struct {
 	Bind                         *url.URL            `help:"Socket to bind to." default:"http://localhost:8892" env:"FTL_CONTROLLER_BIND"`
+	IngressBind                  *url.URL            `help:"Socket to bind to for ingress." default:"http://localhost:8891" env:"FTL_CONTROLLER_INGRESS_BIND"`
 	Key                          model.ControllerKey `help:"Controller key (auto)."`
 	DSN                          string              `help:"DAL DSN." default:"postgres://localhost:54320/ftl?sslmode=disable&user=postgres&password=secret" env:"FTL_CONTROLLER_DSN"`
 	Advertise                    *url.URL            `help:"Endpoint the Controller should advertise (must be unique across the cluster, defaults to --bind if omitted)." env:"FTL_CONTROLLER_ADVERTISE"`
@@ -128,18 +131,26 @@ func Start(ctx context.Context, config Config, runnerScaling scaling.RunnerScali
 
 	console := NewConsoleService(dal)
 
-	ingressHandler := http.StripPrefix("/ingress", svc)
+	ingressHandler := http.Handler(svc)
 	if len(config.AllowOrigins) > 0 {
 		ingressHandler = cors.Middleware(slices.Map(config.AllowOrigins, func(u *url.URL) string { return u.String() }), ingressHandler)
 	}
 
-	return rpc.Serve(ctx, config.Bind,
-		rpc.GRPC(ftlv1connect.NewVerbServiceHandler, svc),
-		rpc.GRPC(ftlv1connect.NewControllerServiceHandler, svc),
-		rpc.GRPC(pbconsoleconnect.NewConsoleServiceHandler, console),
-		rpc.HTTP("/ingress/", ingressHandler),
-		rpc.HTTP("/", consoleHandler),
-	)
+	g, ctx := errgroup.WithContext(ctx)
+	g.Go(func() error {
+		return ftlhttp.Serve(ctx, config.IngressBind, ingressHandler)
+	})
+
+	g.Go(func() error {
+		return rpc.Serve(ctx, config.Bind,
+			rpc.GRPC(ftlv1connect.NewVerbServiceHandler, svc),
+			rpc.GRPC(ftlv1connect.NewControllerServiceHandler, svc),
+			rpc.GRPC(pbconsoleconnect.NewConsoleServiceHandler, console),
+			rpc.HTTP("/", consoleHandler),
+		)
+	})
+
+	return g.Wait()
 }
 
 var _ ftlv1connect.ControllerServiceHandler = (*Service)(nil)
diff --git a/cmd/ftl/cmd_serve.go b/cmd/ftl/cmd_serve.go
index 27bfd9e1d2..8beb4f5f1a 100644
--- a/cmd/ftl/cmd_serve.go
+++ b/cmd/ftl/cmd_serve.go
@@ -31,6 +31,7 @@ import (
 
 type serveCmd struct {
 	Bind           *url.URL      `help:"Starting endpoint to bind to and advertise to. Each controller and runner will increment the port by 1" default:"http://localhost:8892"`
+	IngressBind    *url.URL      `help:"Starting endpoint to bind to for http ingress" default:"http://localhost:8891"`
 	DBPort         int           `help:"Port to use for the database." default:"54320"`
 	Recreate       bool          `help:"Recreate the database even if it already exists." default:"false"`
 	Controllers    int           `short:"c" help:"Number of controllers to start." default:"1"`
@@ -101,6 +102,7 @@ func (s *serveCmd) Run(ctx context.Context) error {
 		config := controller.Config{
 			CommonConfig: s.CommonConfig,
 			Bind:         controllerAddresses[i],
+			IngressBind:  s.IngressBind,
 			Key:          model.NewLocalControllerKey(i),
 			DSN:          dsn,
 		}
diff --git a/frontend/src/features/verbs/verb.utils.ts b/frontend/src/features/verbs/verb.utils.ts
index b5b6fac265..412a52a39d 100644
--- a/frontend/src/features/verbs/verb.utils.ts
+++ b/frontend/src/features/verbs/verb.utils.ts
@@ -3,7 +3,7 @@ import { Module, Verb } from '../../protos/xyz/block/ftl/v1/console/console_pb'
 import { MetadataCalls, MetadataCronJob, MetadataIngress, Ref } from '../../protos/xyz/block/ftl/v1/schema/schema_pb'
 import { JSONSchemaFaker } from 'json-schema-faker'
 
-const basePath = 'http://localhost:8892/ingress/'
+const basePath = 'http://localhost:8891/'
 
 export const verbRefString = (verb: Ref): string => {
   return `${verb.module}.${verb.name}`
diff --git a/integration/actions.go b/integration/actions.go
index 0c96b1eadf..fec8777ee1 100644
--- a/integration/actions.go
+++ b/integration/actions.go
@@ -352,7 +352,7 @@ func JsonData(t testing.TB, body interface{}) []byte {
 func HttpCall(method string, path string, body []byte, onResponse func(t testing.TB, resp *HTTPResponse)) Action {
 	return func(t testing.TB, ic TestContext) {
 		Infof("HTTP %s %s", method, path)
-		baseURL, err := url.Parse(fmt.Sprintf("http://localhost:8892/ingress"))
+		baseURL, err := url.Parse(fmt.Sprintf("http://localhost:8891"))
 		assert.NoError(t, err)
 
 		r, err := http.NewRequestWithContext(ic, method, baseURL.JoinPath(path).String(), bytes.NewReader(body))
diff --git a/internal/http/server.go b/internal/http/server.go
new file mode 100644
index 0000000000..eca4ccac80
--- /dev/null
+++ b/internal/http/server.go
@@ -0,0 +1,45 @@
+package http
+
+import (
+	"context"
+	"errors"
+	"net"
+	"net/http"
+	"net/url"
+	"time"
+
+	"github.com/TBD54566975/ftl/internal/log"
+)
+
+const ShutdownGracePeriod = 5 * time.Second
+
+func Serve(ctx context.Context, listen *url.URL, handler http.Handler) error {
+	httpServer := &http.Server{
+		Addr:              listen.Host,
+		Handler:           handler,
+		ReadHeaderTimeout: 30 * time.Second,
+		BaseContext: func(_ net.Listener) context.Context {
+			return ctx
+		},
+	}
+
+	go func() {
+		<-ctx.Done()
+		shutdownCtx, cancel := context.WithTimeout(context.Background(), ShutdownGracePeriod)
+		defer cancel()
+		err := httpServer.Shutdown(shutdownCtx)
+		if err != nil {
+			if errors.Is(err, context.Canceled) {
+				_ = httpServer.Close()
+				return
+			}
+			log.FromContext(ctx).Errorf(err, "server shutdown error")
+		}
+	}()
+
+	err := httpServer.ListenAndServe()
+	if errors.Is(err, http.ErrServerClosed) {
+		return nil
+	}
+	return err
+}