diff --git a/internal/ingress/controller/template/template.go b/internal/ingress/controller/template/template.go
index 39cfa5ddb..ff4ca1e5b 100644
--- a/internal/ingress/controller/template/template.go
+++ b/internal/ingress/controller/template/template.go
@@ -155,6 +155,7 @@ var (
 		"buildOpentracing":            buildOpentracing,
 		"proxySetHeader":              proxySetHeader,
 		"buildInfluxDB":               buildInfluxDB,
+		"atLeastOneNeedsRewrite":      atLeastOneNeedsRewrite,
 	}
 )
 
@@ -287,9 +288,32 @@ func buildResolvers(res interface{}, disableIpv6 interface{}) string {
 	return strings.Join(r, " ") + ";"
 }
 
+func needsRewrite(location *ingress.Location) bool {
+	if len(location.Rewrite.Target) > 0 && location.Rewrite.Target != location.Path {
+		return true
+	}
+	return false
+}
+
+// atLeastOneNeedsRewrite checks if the nginx.ingress.kubernetes.io/rewrite-target annotation is used on the '/' path
+func atLeastOneNeedsRewrite(input interface{}) bool {
+	locations, ok := input.([]*ingress.Location)
+	if !ok {
+		glog.Errorf("expected an '[]*ingress.Location' type but %T was returned", input)
+		return false
+	}
+
+	for _, location := range locations {
+		if needsRewrite(location) {
+			return true
+		}
+	}
+	return false
+}
+
 // buildLocation produces the location string, if the ingress has redirects
 // (specified through the nginx.ingress.kubernetes.io/rewrite-target annotation)
-func buildLocation(input interface{}) string {
+func buildLocation(input interface{}, rewrite bool) string {
 	location, ok := input.(*ingress.Location)
 	if !ok {
 		glog.Errorf("expected an '*ingress.Location' type but %T was returned", input)
@@ -297,7 +321,7 @@ func buildLocation(input interface{}) string {
 	}
 
 	path := location.Path
-	if len(location.Rewrite.Target) > 0 && location.Rewrite.Target != path {
+	if needsRewrite(location) {
 		if path == slash {
 			return fmt.Sprintf("~* %s", path)
 		}
@@ -310,6 +334,12 @@ func buildLocation(input interface{}) string {
 		return fmt.Sprintf(`~* ^%s%s`, path, baseuri)
 	}
 
+	if rewrite {
+		if path == slash {
+			return path
+		}
+		return fmt.Sprintf(`^~ %s`, path)
+	}
 	return path
 }
 
diff --git a/internal/ingress/controller/template/template_test.go b/internal/ingress/controller/template/template_test.go
index 7068d295e..5e489d867 100644
--- a/internal/ingress/controller/template/template_test.go
+++ b/internal/ingress/controller/template/template_test.go
@@ -50,6 +50,7 @@ var (
 		XForwardedPrefix            bool
 		DynamicConfigurationEnabled bool
 		SecureBackend               bool
+		atLeastOneNeedsRewrite      bool
 	}{
 		"when secure backend enabled": {
 			"/",
@@ -61,7 +62,8 @@ var (
 			false,
 			false,
 			false,
-			true},
+			true,
+			false},
 		"when secure backend and stickeness enabled": {
 			"/",
 			"/",
@@ -72,7 +74,8 @@ var (
 			true,
 			false,
 			false,
-			true},
+			true,
+			false},
 		"when secure backend and dynamic config enabled": {
 			"/",
 			"/",
@@ -83,7 +86,8 @@ var (
 			false,
 			false,
 			true,
-			true},
+			true,
+			false},
 		"when secure backend, stickeness and dynamic config enabled": {
 			"/",
 			"/",
@@ -94,7 +98,8 @@ var (
 			true,
 			false,
 			true,
-			true},
+			true,
+			false},
 		"invalid redirect / to / with dynamic config enabled": {
 			"/",
 			"/",
@@ -105,6 +110,7 @@ var (
 			false,
 			false,
 			true,
+			false,
 			false},
 		"invalid redirect / to /": {
 			"/",
@@ -116,6 +122,7 @@ var (
 			false,
 			false,
 			false,
+			false,
 			false},
 		"redirect / to /jenkins": {
 			"/",
@@ -131,7 +138,8 @@ proxy_pass http://upstream-name;
 			false,
 			false,
 			false,
-			false},
+			false,
+			true},
 		"redirect /something to /": {
 			"/something",
 			"/",
@@ -146,7 +154,8 @@ proxy_pass http://upstream-name;
 			false,
 			false,
 			false,
-			false},
+			false,
+			true},
 		"redirect /end-with-slash/ to /not-root": {
 			"/end-with-slash/",
 			"/not-root",
@@ -161,7 +170,8 @@ proxy_pass http://upstream-name;
 			false,
 			false,
 			false,
-			false},
+			false,
+			true},
 		"redirect /something-complex to /not-root": {
 			"/something-complex",
 			"/not-root",
@@ -176,7 +186,8 @@ proxy_pass http://upstream-name;
 			false,
 			false,
 			false,
-			false},
+			false,
+			true},
 		"redirect / to /jenkins and rewrite": {
 			"/",
 			"/jenkins",
@@ -194,7 +205,8 @@ subs_filter '(<(?:H|h)(?:E|e)(?:A|a)(?:D|d)(?:[^">]|"[^"]*")*>)' '$1<base href="
 			false,
 			false,
 			false,
-			false},
+			false,
+			true},
 		"redirect /something to / and rewrite": {
 			"/something",
 			"/",
@@ -212,7 +224,8 @@ subs_filter '(<(?:H|h)(?:E|e)(?:A|a)(?:D|d)(?:[^">]|"[^"]*")*>)' '$1<base href="
 			false,
 			false,
 			false,
-			false},
+			false,
+			true},
 		"redirect /end-with-slash/ to /not-root and rewrite": {
 			"/end-with-slash/",
 			"/not-root",
@@ -230,7 +243,8 @@ subs_filter '(<(?:H|h)(?:E|e)(?:A|a)(?:D|d)(?:[^">]|"[^"]*")*>)' '$1<base href="
 			false,
 			false,
 			false,
-			false},
+			false,
+			true},
 		"redirect /something-complex to /not-root and rewrite": {
 			"/something-complex",
 			"/not-root",
@@ -248,7 +262,8 @@ subs_filter '(<(?:H|h)(?:E|e)(?:A|a)(?:D|d)(?:[^">]|"[^"]*")*>)' '$1<base href="
 			false,
 			false,
 			false,
-			false},
+			false,
+			true},
 		"redirect /something to / and rewrite with specific scheme": {
 			"/something",
 			"/",
@@ -266,7 +281,8 @@ subs_filter '(<(?:H|h)(?:E|e)(?:A|a)(?:D|d)(?:[^">]|"[^"]*")*>)' '$1<base href="
 			false,
 			false,
 			false,
-			false},
+			false,
+			true},
 		"redirect / to /something with sticky enabled": {
 			"/",
 			"/something",
@@ -281,7 +297,8 @@ proxy_pass http://sticky-upstream-name;
 			true,
 			false,
 			false,
-			false},
+			false,
+			true},
 		"redirect / to /something with sticky and dynamic config enabled": {
 			"/",
 			"/something",
@@ -296,7 +313,8 @@ proxy_pass http://upstream_balancer;
 			true,
 			false,
 			true,
-			false},
+			false,
+			true},
 		"add the X-Forwarded-Prefix header": {
 			"/there",
 			"/something",
@@ -312,7 +330,32 @@ proxy_pass http://sticky-upstream-name;
 			true,
 			true,
 			false,
-			false},
+			false,
+			true},
+		"do not use ^~ location modifier on index when ingress does not use rewrite target but at least one other ingress does": {
+			"/",
+			"/",
+			"/",
+			"proxy_pass http://upstream-name;",
+			false,
+			"",
+			false,
+			false,
+			false,
+			false,
+			true},
+		"use ^~ location modifier when ingress does not use rewrite target but at least one other ingress does": {
+			"/something",
+			"/something",
+			"^~ /something",
+			"proxy_pass http://upstream-name;",
+			false,
+			"",
+			false,
+			false,
+			false,
+			false,
+			true},
 	}
 )
 
@@ -382,7 +425,7 @@ func TestBuildLocation(t *testing.T) {
 			Rewrite: rewrite.Config{Target: tc.Target, AddBaseURL: tc.AddBaseURL},
 		}
 
-		newLoc := buildLocation(loc)
+		newLoc := buildLocation(loc, tc.atLeastOneNeedsRewrite)
 		if tc.Location != newLoc {
 			t.Errorf("%s: expected '%v' but returned %v", k, tc.Location, newLoc)
 		}
diff --git a/rootfs/etc/nginx/template/nginx.tmpl b/rootfs/etc/nginx/template/nginx.tmpl
index 027010882..915ce66a7 100644
--- a/rootfs/etc/nginx/template/nginx.tmpl
+++ b/rootfs/etc/nginx/template/nginx.tmpl
@@ -452,8 +452,9 @@ http {
 
     {{/* build the maps that will be use to validate the Whitelist */}}
     {{ range $server := $servers }}
+    {{ $usesRewrite := atLeastOneNeedsRewrite $server.Locations }}
     {{ range $location := $server.Locations }}
-    {{ $path := buildLocation $location }}
+    {{ $path := buildLocation $location $usesRewrite }}
 
     {{ if isLocationAllowed $location }}
     {{ if gt (len $location.Whitelist.CIDR) 0 }}
@@ -818,8 +819,9 @@ stream {
         {{ $server.ServerSnippet }}
         {{ end }}
 
+        {{ $usesRewrite := atLeastOneNeedsRewrite $server.Locations }}
         {{ range $location := $server.Locations }}
-        {{ $path := buildLocation $location }}
+        {{ $path := buildLocation $location $usesRewrite }}
         {{ $proxySetHeader := proxySetHeader $location }}
         {{ $authPath := buildAuthLocation $location }}
 
diff --git a/test/e2e/annotations/rewrite.go b/test/e2e/annotations/rewrite.go
index 07cf8f845..47118355c 100644
--- a/test/e2e/annotations/rewrite.go
+++ b/test/e2e/annotations/rewrite.go
@@ -117,4 +117,56 @@ var _ = framework.IngressNginxDescribe("Annotations - Rewrite", func() {
 		Expect(logs).To(ContainSubstring(`"(?i)/something$" matches "/something", client:`))
 		Expect(logs).To(ContainSubstring(`rewritten data: "/", args: "",`))
 	})
+
+	It("should use correct longest path match", func() {
+		host := "rewrite.bar.com"
+		expectBodyRequestURI := fmt.Sprintf("request_uri=http://%v:8080/.well-known/acme/challenge", host)
+
+		By("creating a regular ingress definition")
+		ing := framework.NewSingleIngress("kube-lego", "/.well-known/acme/challenge", host, f.IngressController.Namespace, "http-svc", 80, &map[string]string{})
+		_, err := f.EnsureIngress(ing)
+		Expect(err).NotTo(HaveOccurred())
+		Expect(ing).NotTo(BeNil())
+
+		err = f.WaitForNginxServer(host,
+			func(server string) bool {
+				return strings.Contains(server, "/.well-known/acme/challenge")
+			})
+		Expect(err).NotTo(HaveOccurred())
+
+		By("making a request to the non-rewritten location")
+		resp, body, errs := gorequest.New().
+			Get(f.IngressController.HTTPURL+"/.well-known/acme/challenge").
+			Set("Host", host).
+			End()
+
+		Expect(len(errs)).Should(Equal(0))
+		Expect(resp.StatusCode).Should(Equal(http.StatusOK))
+		Expect(body).Should(ContainSubstring(expectBodyRequestURI))
+
+		By(`creating an ingress definition with the rewrite-target annotation set on the "/" location`)
+		annotations := map[string]string{
+			"nginx.ingress.kubernetes.io/rewrite-target": "/new/backend",
+		}
+		rewriteIng := framework.NewSingleIngress("rewrite-index", "/", host, f.IngressController.Namespace, "http-svc", 80, &annotations)
+		_, err = f.EnsureIngress(rewriteIng)
+		Expect(err).NotTo(HaveOccurred())
+		Expect(rewriteIng).NotTo(BeNil())
+
+		err = f.WaitForNginxServer(host,
+			func(server string) bool {
+				return strings.Contains(server, "location ~* / {")
+			})
+		Expect(err).NotTo(HaveOccurred())
+
+		By("making a second request to the non-rewritten location")
+		resp, body, errs = gorequest.New().
+			Get(f.IngressController.HTTPURL+"/.well-known/acme/challenge").
+			Set("Host", host).
+			End()
+
+		Expect(len(errs)).Should(Equal(0))
+		Expect(resp.StatusCode).Should(Equal(http.StatusOK))
+		Expect(body).Should(ContainSubstring(expectBodyRequestURI))
+	})
 })