diff --git a/cmd/cloudflared/tunnel/cmd.go b/cmd/cloudflared/tunnel/cmd.go
index 46f11fd0..a54fd686 100644
--- a/cmd/cloudflared/tunnel/cmd.go
+++ b/cmd/cloudflared/tunnel/cmd.go
@@ -128,7 +128,7 @@ func Commands() []*cli.Command {
 		dbConnectCmd(),
 	}
 
-	return []*cli.Command {
+	return []*cli.Command{
 		buildTunnelCommand(subcommands),
 		// for compatibility, allow following as top-level subcommands
 		buildLoginSubcommand(true),
diff --git a/cmd/cloudflared/tunnel/configuration.go b/cmd/cloudflared/tunnel/configuration.go
index 0490269d..c91d1008 100644
--- a/cmd/cloudflared/tunnel/configuration.go
+++ b/cmd/cloudflared/tunnel/configuration.go
@@ -232,16 +232,17 @@ func prepareTunnelConfig(
 			Arch:     fmt.Sprintf("%s_%s", buildInfo.GoOS, buildInfo.GoArch),
 		}
 		ingressRules, err = config.ReadRules(c)
-		if err != nil {
+		if err != nil && err != ingress.ErrNoIngressRules {
 			return nil, err
 		}
-		if c.IsSet("url") {
+		if len(ingressRules) > 0 && c.IsSet("url") {
 			return nil, ingress.ErrURLIncompatibleWithIngress
 		}
 	}
 
 	var originURL string
-	if len(ingressRules) == 0 {
+	isUsingMultipleOrigins := len(ingressRules) > 0
+	if !isUsingMultipleOrigins {
 		originURL, err = config.ValidateUrl(c, compatibilityMode)
 		if err != nil {
 			logger.Errorf("Error validating origin URL: %s", err)
@@ -271,8 +272,22 @@ func prepareTunnelConfig(
 	}
 	// If tunnel running in bastion mode, a connection to origin will not exist until initiated by the client.
 	if !c.IsSet(bastionFlag) {
-		if err = validation.ValidateHTTPService(originURL, hostname, httpTransport); err != nil {
-			logger.Errorf("unable to connect to the origin: %s", err)
+
+		// List all origin URLs that require validation
+		var originURLs []string
+		if !isUsingMultipleOrigins {
+			originURLs = append(originURLs, originURL)
+		} else {
+			for _, rule := range ingressRules {
+				originURLs = append(originURLs, rule.Service.String())
+			}
+		}
+
+		// Validate each origin URL
+		for _, u := range originURLs {
+			if err = validation.ValidateHTTPService(u, hostname, httpTransport); err != nil {
+				logger.Errorf("unable to connect to the origin: %s", err)
+			}
 		}
 	}
 
diff --git a/ingress/ingress.go b/ingress/ingress.go
index fcfab77d..3489bbcb 100644
--- a/ingress/ingress.go
+++ b/ingress/ingress.go
@@ -11,7 +11,7 @@ import (
 )
 
 var (
-	errNoIngressRules             = errors.New("No ingress rules were specified in the config file")
+	ErrNoIngressRules             = errors.New("No ingress rules were specified in the config file")
 	errLastRuleNotCatchAll        = errors.New("The last ingress rule must match all hostnames (i.e. it must be missing, or must be \"*\")")
 	errBadWildcard                = errors.New("Hostname patterns can have at most one wildcard character (\"*\") and it can only be used for subdomains, e.g. \"*.example.com\"")
 	errNoIngressRulesMatch        = errors.New("The URL didn't match any ingress rules")
@@ -50,12 +50,24 @@ func (r Rule) String() string {
 	return out.String()
 }
 
-func (r Rule) matches(requestURL *url.URL) bool {
-	hostMatch := r.Hostname == "" || r.Hostname == "*" || matchHost(r.Hostname, requestURL.Hostname())
-	pathMatch := r.Path == nil || r.Path.MatchString(requestURL.Path)
+func (r *Rule) Matches(hostname, path string) bool {
+	hostMatch := r.Hostname == "" || r.Hostname == "*" || matchHost(r.Hostname, hostname)
+	pathMatch := r.Path == nil || r.Path.MatchString(path)
 	return hostMatch && pathMatch
 }
 
+// FindMatchingRule returns the index of the Ingress Rule which matches the given
+// hostname and path. This function assumes the last rule matches everything,
+// which is the case if the rules were instantiated via the ingress#Validate method
+func FindMatchingRule(hostname, path string, rules []Rule) int {
+	for i, rule := range rules {
+		if rule.Matches(hostname, path) {
+			return i
+		}
+	}
+	return len(rules) - 1
+}
+
 func matchHost(ruleHost, reqHost string) bool {
 	if ruleHost == reqHost {
 		return true
@@ -94,6 +106,10 @@ func (ing ingress) validate() ([]Rule, error) {
 			return nil, fmt.Errorf("The service %s must have a scheme and a hostname", r.Service)
 		}
 
+		if service.Path != "" {
+			return nil, fmt.Errorf("%s is an invalid address, ingress rules don't support proxying to a different path on the origin service. The path will be the same as the eyeball request's path.", r.Service)
+		}
+
 		// Ensure that there are no wildcards anywhere except the first character
 		// of the hostname.
 		if strings.LastIndex(r.Hostname, "*") > 0 {
@@ -145,7 +161,7 @@ func ParseIngress(rawYAML []byte) ([]Rule, error) {
 		return nil, err
 	}
 	if len(ing.Ingress) == 0 {
-		return nil, errNoIngressRules
+		return nil, ErrNoIngressRules
 	}
 	return ing.validate()
 }
@@ -155,12 +171,8 @@ func RuleCommand(rules []Rule, requestURL *url.URL) error {
 	if requestURL.Hostname() == "" {
 		return fmt.Errorf("%s is malformed and doesn't have a hostname", requestURL)
 	}
-	for i, r := range rules {
-		if r.matches(requestURL) {
-			fmt.Printf("Matched rule #%d\n", i+1)
-			fmt.Println(r.String())
-			return nil
-		}
-	}
-	return errNoIngressRulesMatch
+	i := FindMatchingRule(requestURL.Hostname(), requestURL.Path, rules)
+	fmt.Printf("Matched rule #%d\n", i+1)
+	fmt.Println(rules[i].String())
+	return nil
 }
diff --git a/ingress/ingress_test.go b/ingress/ingress_test.go
index 1d5cd379..99450a0c 100644
--- a/ingress/ingress_test.go
+++ b/ingress/ingress_test.go
@@ -135,6 +135,33 @@ ingress:
 			args: args{rawYAML: `
 ingress:
   - service: localhost:8000
+`},
+			wantErr: true,
+		},
+		{
+			name: "Wildcard not at start",
+			args: args{rawYAML: `
+ingress:
+  - hostname: "test.*.example.com"
+    service: https://localhost:8000
+`},
+			wantErr: true,
+		},
+		{
+			name: "Can't use --url",
+			args: args{rawYAML: `
+url: localhost:8080
+ingress:
+  - hostname: "*.example.com"
+    service: https://localhost:8000
+`},
+			wantErr: true,
+		},
+		{
+			name: "Service can't have a path",
+			args: args{rawYAML: `
+ingress:
+  - service: https://localhost:8000/static/
 `},
 			wantErr: true,
 		},
@@ -263,9 +290,31 @@ func Test_rule_matches(t *testing.T) {
 				Path:     tt.fields.Path,
 				Service:  tt.fields.Service,
 			}
-			if got := r.matches(tt.args.requestURL); got != tt.want {
+			u := tt.args.requestURL
+			if got := r.Matches(u.Hostname(), u.Path); got != tt.want {
 				t.Errorf("rule.matches() = %v, want %v", got, tt.want)
 			}
 		})
 	}
 }
+
+func BenchmarkFindMatch(b *testing.B) {
+	rulesYAML := `
+ingress:
+  - hostname: tunnel1.example.com
+    service: https://localhost:8000
+  - hostname: tunnel2.example.com
+    service: https://localhost:8001
+  - hostname: "*"
+    service: https://localhost:8002
+`
+	rules, err := ParseIngress([]byte(rulesYAML))
+	if err != nil {
+		b.Error(err)
+	}
+	for n := 0; n < b.N; n++ {
+		FindMatchingRule("tunnel1.example.com", "", rules)
+		FindMatchingRule("tunnel2.example.com", "", rules)
+		FindMatchingRule("tunnel3.example.com", "", rules)
+	}
+}
diff --git a/origin/tunnel.go b/origin/tunnel.go
index b9ea8c1e..997ea779 100644
--- a/origin/tunnel.go
+++ b/origin/tunnel.go
@@ -619,6 +619,7 @@ func LogServerInfo(
 
 type TunnelHandler struct {
 	originUrl      string
+	ingressRules   []ingress.Rule
 	httpHostHeader string
 	muxer          *h2mux.Muxer
 	httpClient     http.RoundTripper
@@ -640,12 +641,20 @@ func NewTunnelHandler(ctx context.Context,
 	connectionID uint8,
 	bufferPool *buffer.Pool,
 ) (*TunnelHandler, string, error) {
-	originURL, err := validation.ValidateUrl(config.OriginUrl)
-	if err != nil {
-		return nil, "", fmt.Errorf("unable to parse origin URL %#v", originURL)
+
+	// Check single-origin config
+	var originURL string
+	var err error
+	if len(config.IngressRules) == 0 {
+		originURL, err = validation.ValidateUrl(config.OriginUrl)
+		if err != nil {
+			return nil, "", fmt.Errorf("unable to parse origin URL %#v", originURL)
+		}
 	}
+
 	h := &TunnelHandler{
 		originUrl:         originURL,
+		ingressRules:      config.IngressRules,
 		httpHostHeader:    config.HTTPHostHeader,
 		httpClient:        config.HTTPTransport,
 		tlsConfig:         config.ClientTlsConfig,
@@ -718,6 +727,12 @@ func (h *TunnelHandler) createRequest(stream *h2mux.MuxedStream) (*http.Request,
 		return nil, errors.Wrap(err, "invalid request received")
 	}
 	h.AppendTagHeaders(req)
+	if len(h.ingressRules) > 0 {
+		ruleNumber := ingress.FindMatchingRule(req.Host, req.URL.Path, h.ingressRules)
+		destination := h.ingressRules[ruleNumber].Service
+		req.URL.Host = destination.Host
+		req.URL.Scheme = destination.Scheme
+	}
 	return req, nil
 }