diff --git a/internal/dag/builder_test.go b/internal/dag/builder_test.go
index e56679492a7..cc187bcba42 100644
--- a/internal/dag/builder_test.go
+++ b/internal/dag/builder_test.go
@@ -1762,6 +1762,106 @@ func TestDAGInsert(t *testing.T) {
 		},
 	}
 
+	// proxy2d is a proxy with two routes that have the same prefix and a Contains header
+	// condition on the same header, differing only in the value of the condition.
+	proxy2d := &projcontour.HTTPProxy{
+		ObjectMeta: metav1.ObjectMeta{
+			Name:      "example-com",
+			Namespace: "default",
+		},
+		Spec: projcontour.HTTPProxySpec{
+			VirtualHost: &projcontour.VirtualHost{
+				Fqdn: "example.com",
+			},
+			Routes: []projcontour.Route{
+				{
+					Conditions: []projcontour.Condition{
+						{
+							Header: &projcontour.HeaderCondition{
+								Name:     "e-tag",
+								Contains: "abc",
+							},
+						},
+						{
+							Prefix: "/",
+						},
+					},
+					Services: []projcontour.Service{{
+						Name: "kuard",
+						Port: 8080,
+					}},
+				},
+				{
+					Conditions: []projcontour.Condition{
+						{
+							Header: &projcontour.HeaderCondition{
+								Name:     "e-tag",
+								Contains: "def",
+							},
+						},
+						{
+							Prefix: "/",
+						},
+					},
+					Services: []projcontour.Service{{
+						Name: "kuard",
+						Port: 8080,
+					}},
+				},
+			},
+		},
+	}
+
+	// proxy2e is a proxy with two routes that both have a condition on the same
+	// header, one using Contains and one using NotContains.
+	proxy2e := &projcontour.HTTPProxy{
+		ObjectMeta: metav1.ObjectMeta{
+			Name:      "example-com",
+			Namespace: "default",
+		},
+		Spec: projcontour.HTTPProxySpec{
+			VirtualHost: &projcontour.VirtualHost{
+				Fqdn: "example.com",
+			},
+			Routes: []projcontour.Route{
+				{
+					Conditions: []projcontour.Condition{
+						{
+							Header: &projcontour.HeaderCondition{
+								Name:     "e-tag",
+								Contains: "abc",
+							},
+						},
+						{
+							Prefix: "/",
+						},
+					},
+					Services: []projcontour.Service{{
+						Name: "kuard",
+						Port: 8080,
+					}},
+				},
+				{
+					Conditions: []projcontour.Condition{
+						{
+							Header: &projcontour.HeaderCondition{
+								Name:        "e-tag",
+								NotContains: "abc",
+							},
+						},
+						{
+							Prefix: "/",
+						},
+					},
+					Services: []projcontour.Service{{
+						Name: "kuard",
+						Port: 8080,
+					}},
+				},
+			},
+		},
+	}
+
 	// proxy6 has TLS and does not specify min tls version
 	proxy6 := &projcontour.HTTPProxy{
 		ObjectMeta: metav1.ObjectMeta{
@@ -4231,6 +4331,56 @@ func TestDAGInsert(t *testing.T) {
 				},
 			),
 		},
+		"insert httproxy w/ multiple routes with a Contains condition on the same header": {
+			objs: []interface{}{
+				proxy2d, s1,
+			},
+			want: listeners(
+				&Listener{
+					Port: 80,
+					VirtualHosts: virtualhosts(
+						virtualhost("example.com", &Route{
+							PathCondition: &PrefixCondition{Prefix: "/"},
+							HeaderConditions: []HeaderCondition{
+								{Name: "e-tag", Value: "abc", MatchType: "contains"},
+							},
+							Clusters: clusters(service(s1)),
+						}, &Route{
+							PathCondition: &PrefixCondition{Prefix: "/"},
+							HeaderConditions: []HeaderCondition{
+								{Name: "e-tag", Value: "def", MatchType: "contains"},
+							},
+							Clusters: clusters(service(s1)),
+						}),
+					),
+				},
+			),
+		},
+		"insert httproxy w/ multiple routes with condition on the same header, one Contains and one NotContains": {
+			objs: []interface{}{
+				proxy2e, s1,
+			},
+			want: listeners(
+				&Listener{
+					Port: 80,
+					VirtualHosts: virtualhosts(
+						virtualhost("example.com", &Route{
+							PathCondition: &PrefixCondition{Prefix: "/"},
+							HeaderConditions: []HeaderCondition{
+								{Name: "e-tag", Value: "abc", MatchType: "contains"},
+							},
+							Clusters: clusters(service(s1)),
+						}, &Route{
+							PathCondition: &PrefixCondition{Prefix: "/"},
+							HeaderConditions: []HeaderCondition{
+								{Name: "e-tag", Value: "abc", MatchType: "contains", Invert: true},
+							},
+							Clusters: clusters(service(s1)),
+						}),
+					),
+				},
+			),
+		},
 		"insert httproxy w/ included conditions": {
 			objs: []interface{}{
 				proxy2a, proxy2b, s1,
diff --git a/internal/dag/dag.go b/internal/dag/dag.go
index 1de2d76ca94..a6fa83b57eb 100644
--- a/internal/dag/dag.go
+++ b/internal/dag/dag.go
@@ -17,6 +17,7 @@ package dag
 
 import (
 	"fmt"
+	"strconv"
 	"strings"
 	"time"
 
@@ -79,7 +80,14 @@ type HeaderCondition struct {
 }
 
 func (hc *HeaderCondition) String() string {
-	return "header: " + hc.Name
+	details := strings.Join([]string{
+		"name=" + hc.Name,
+		"value=" + hc.Value,
+		"matchtype=", hc.MatchType,
+		"invert=", strconv.FormatBool(hc.Invert),
+	}, "&")
+
+	return "header: " + details
 }
 
 // Route defines the properties of a route to a Cluster.
diff --git a/internal/featuretests/headercondition_test.go b/internal/featuretests/headercondition_test.go
index dfdc8f30582..366a974e976 100644
--- a/internal/featuretests/headercondition_test.go
+++ b/internal/featuretests/headercondition_test.go
@@ -388,4 +388,122 @@ func TestConditions_ContainsHeader_HTTProxy(t *testing.T) {
 		),
 		TypeUrl: routeType,
 	})
+
+	// proxy with two routes that have the same prefix and a Contains header
+	// condition on the same header, differing only in the value of the condition.
+	proxy6 := fixture.NewProxy("simple").WithSpec(
+		projcontour.HTTPProxySpec{
+			VirtualHost: &projcontour.VirtualHost{Fqdn: "hello.world"},
+			Routes: []projcontour.Route{
+				{
+					Conditions: conditions(
+						prefixCondition("/"),
+						headerContainsCondition("x-header", "abc"),
+					),
+					Services: []projcontour.Service{{
+						Name: "svc1",
+						Port: 80,
+					}},
+				},
+				{
+					Conditions: conditions(
+						prefixCondition("/"),
+						headerContainsCondition("x-header", "def"),
+					),
+					Services: []projcontour.Service{{
+						Name: "svc2",
+						Port: 80,
+					}},
+				}},
+		},
+	)
+
+	rh.OnUpdate(proxy5, proxy6)
+
+	c.Request(routeType).Equals(&v2.DiscoveryResponse{
+		Resources: resources(t,
+			envoy.RouteConfiguration("ingress_http",
+				envoy.VirtualHost("hello.world",
+					&envoy_api_v2_route.Route{
+						Match: routePrefix("/", dag.HeaderCondition{
+							Name:      "x-header",
+							Value:     "abc",
+							MatchType: "contains",
+							Invert:    false,
+						}),
+						Action: routeCluster("default/svc1/80/da39a3ee5e"),
+					},
+					&envoy_api_v2_route.Route{
+						Match: routePrefix("/", dag.HeaderCondition{
+							Name:      "x-header",
+							Value:     "def",
+							MatchType: "contains",
+							Invert:    false,
+						}),
+						Action: routeCluster("default/svc2/80/da39a3ee5e"),
+					},
+				),
+			),
+		),
+		TypeUrl: routeType,
+	})
+
+	// proxy with two routes that both have a condition on the same
+	// header, one using Contains and one using NotContains.
+	proxy7 := fixture.NewProxy("simple").WithSpec(
+		projcontour.HTTPProxySpec{
+			VirtualHost: &projcontour.VirtualHost{Fqdn: "hello.world"},
+			Routes: []projcontour.Route{
+				{
+					Conditions: conditions(
+						prefixCondition("/"),
+						headerContainsCondition("x-header", "abc"),
+					),
+					Services: []projcontour.Service{{
+						Name: "svc1",
+						Port: 80,
+					}},
+				},
+				{
+					Conditions: conditions(
+						prefixCondition("/"),
+						headerNotContainsCondition("x-header", "abc"),
+					),
+					Services: []projcontour.Service{{
+						Name: "svc2",
+						Port: 80,
+					}},
+				}},
+		},
+	)
+
+	rh.OnUpdate(proxy6, proxy7)
+
+	c.Request(routeType).Equals(&v2.DiscoveryResponse{
+		Resources: resources(t,
+			envoy.RouteConfiguration("ingress_http",
+				envoy.VirtualHost("hello.world",
+					&envoy_api_v2_route.Route{
+						Match: routePrefix("/", dag.HeaderCondition{
+							Name:      "x-header",
+							Value:     "abc",
+							MatchType: "contains",
+							Invert:    false,
+						}),
+						Action: routeCluster("default/svc1/80/da39a3ee5e"),
+					},
+					&envoy_api_v2_route.Route{
+						Match: routePrefix("/", dag.HeaderCondition{
+							Name:      "x-header",
+							Value:     "abc",
+							MatchType: "contains",
+							Invert:    true,
+						}),
+						Action: routeCluster("default/svc2/80/da39a3ee5e"),
+					},
+				),
+			),
+		),
+		TypeUrl: routeType,
+	})
 }