diff --git a/CHANGELOG.md b/CHANGELOG.md
index 6934aee5143..0cb429b1ead 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -3,6 +3,8 @@
 IMPROVEMENTS:
  * driver/docker: Allow setting container IP with user defined networks
    [GH-2535]
+ * client: Fingerprint all routable addresses on an interface including IPv6
+   addresses [GH-2536]
 
 BUG FIXES:
  * server: Reject non-TLS clients when TLS enabled [GH-2525]
diff --git a/api/resources.go b/api/resources.go
index 14c6a4fd72b..8d3f27c6cd2 100644
--- a/api/resources.go
+++ b/api/resources.go
@@ -66,12 +66,12 @@ type Port struct {
 // NetworkResource is used to describe required network
 // resources of a given task.
 type NetworkResource struct {
-	Public        bool
+	Device        string
 	CIDR          string
-	ReservedPorts []Port
-	DynamicPorts  []Port
 	IP            string
 	MBits         *int
+	ReservedPorts []Port
+	DynamicPorts  []Port
 }
 
 func (n *NetworkResource) Canonicalize() {
diff --git a/client/fingerprint/network.go b/client/fingerprint/network.go
index eceb213e43f..bfc59c7e830 100644
--- a/client/fingerprint/network.go
+++ b/client/fingerprint/network.go
@@ -1,7 +1,6 @@
 package fingerprint
 
 import (
-	"errors"
 	"fmt"
 	"log"
 	"net"
@@ -56,10 +55,11 @@ func NewNetworkFingerprint(logger *log.Logger) Fingerprint {
 }
 
 func (f *NetworkFingerprint) Fingerprint(cfg *config.Config, node *structs.Node) (bool, error) {
-	// newNetwork is populated and addded to the Nodes resources
-	newNetwork := &structs.NetworkResource{}
-	var ip string
+	if node.Resources == nil {
+		node.Resources = &structs.Resources{}
+	}
 
+	// Find the named interface
 	intf, err := f.findInterface(cfg.NetworkInterface)
 	switch {
 	case err != nil:
@@ -69,52 +69,57 @@ func (f *NetworkFingerprint) Fingerprint(cfg *config.Config, node *structs.Node)
 		return false, nil
 	}
 
-	if ip, err = f.ipAddress(intf); err != nil {
-		return false, fmt.Errorf("Unable to find IP address of interface: %s, err: %v", intf.Name, err)
-	}
-
-	newNetwork.Device = intf.Name
-	node.Attributes["unique.network.ip-address"] = ip
-	newNetwork.IP = ip
-	newNetwork.CIDR = newNetwork.IP + "/32"
-
-	f.logger.Printf("[DEBUG] fingerprint.network: Detected interface %v with IP %v during fingerprinting", intf.Name, ip)
-
+	// Record the throughput of the interface
+	var mbits int
 	throughput := f.linkSpeed(intf.Name)
 	if cfg.NetworkSpeed != 0 {
-		newNetwork.MBits = cfg.NetworkSpeed
-		f.logger.Printf("[DEBUG] fingerprint.network: setting link speed to user configured speed: %d", newNetwork.MBits)
+		mbits = cfg.NetworkSpeed
+		f.logger.Printf("[DEBUG] fingerprint.network: setting link speed to user configured speed: %d", mbits)
 	} else if throughput != 0 {
-		newNetwork.MBits = throughput
-		f.logger.Printf("[DEBUG] fingerprint.network: link speed for %v set to %v", intf.Name, newNetwork.MBits)
+		mbits = throughput
+		f.logger.Printf("[DEBUG] fingerprint.network: link speed for %v set to %v", intf.Name, mbits)
 	} else {
-		newNetwork.MBits = defaultNetworkSpeed
+		mbits = defaultNetworkSpeed
 		f.logger.Printf("[DEBUG] fingerprint.network: link speed could not be detected and no speed specified by user. Defaulting to %d", defaultNetworkSpeed)
 	}
 
-	if node.Resources == nil {
-		node.Resources = &structs.Resources{}
+	// Create the network resources from the interface
+	nwResources, err := f.createNetworkResources(mbits, intf)
+	if err != nil {
+		return false, err
 	}
 
-	node.Resources.Networks = append(node.Resources.Networks, newNetwork)
+	// Add the network resources to the node
+	node.Resources.Networks = nwResources
+	for _, nwResource := range nwResources {
+		f.logger.Printf("[DEBUG] fingerprint.network: Detected interface %v with IP: %v", intf.Name, nwResource.IP)
+	}
+
+	// Deprecated, setting the first IP as unique IP for the node
+	if len(nwResources) > 0 {
+		node.Attributes["unique.network.ip-address"] = nwResources[0].IP
+	}
 
 	// return true, because we have a network connection
 	return true, nil
 }
 
-// Gets the ipv4 addr for a network interface
-func (f *NetworkFingerprint) ipAddress(intf *net.Interface) (string, error) {
-	var addrs []net.Addr
-	var err error
-
-	if addrs, err = f.interfaceDetector.Addrs(intf); err != nil {
-		return "", err
-	}
-
-	if len(addrs) == 0 {
-		return "", errors.New(fmt.Sprintf("Interface %s has no IP address", intf.Name))
+// createNetworkResources creates network resources for every IP
+func (f *NetworkFingerprint) createNetworkResources(throughput int, intf *net.Interface) ([]*structs.NetworkResource, error) {
+	// Find the interface with the name
+	addrs, err := f.interfaceDetector.Addrs(intf)
+	if err != nil {
+		return nil, err
 	}
+	nwResources := make([]*structs.NetworkResource, 0)
 	for _, addr := range addrs {
+		// Create a new network resource
+		newNetwork := &structs.NetworkResource{
+			Device: intf.Name,
+			MBits:  throughput,
+		}
+
+		// Find the IP Addr and the CIDR from the Address
 		var ip net.IP
 		switch v := (addr).(type) {
 		case *net.IPNet:
@@ -122,13 +127,21 @@ func (f *NetworkFingerprint) ipAddress(intf *net.Interface) (string, error) {
 		case *net.IPAddr:
 			ip = v.IP
 		}
+
+		// If the ip is link-local then we ignore it
+		if ip.IsLinkLocalUnicast() || ip.IsLinkLocalMulticast() {
+			continue
+		}
+		newNetwork.IP = ip.String()
 		if ip.To4() != nil {
-			return ip.String(), nil
+			newNetwork.CIDR = newNetwork.IP + "/32"
+		} else {
+			newNetwork.CIDR = newNetwork.IP + "/128"
 		}
-	}
-
-	return "", fmt.Errorf("Couldn't parse IP address for interface %s", intf.Name)
 
+		nwResources = append(nwResources, newNetwork)
+	}
+	return nwResources, nil
 }
 
 // Checks if the device is marked UP by the operator
@@ -138,8 +151,8 @@ func (f *NetworkFingerprint) isDeviceEnabled(intf *net.Interface) bool {
 
 // Checks if the device has any IP address configured
 func (f *NetworkFingerprint) deviceHasIpAddress(intf *net.Interface) bool {
-	_, err := f.ipAddress(intf)
-	return err == nil
+	addrs, err := f.interfaceDetector.Addrs(intf)
+	return err == nil && len(addrs) != 0
 }
 
 func (n *NetworkFingerprint) isDeviceLoopBackOrPointToPoint(intf *net.Interface) bool {
diff --git a/client/fingerprint/network_test.go b/client/fingerprint/network_test.go
index 84e0a764228..eaa638b5678 100644
--- a/client/fingerprint/network_test.go
+++ b/client/fingerprint/network_test.go
@@ -126,8 +126,9 @@ func (n *NetworkInterfaceDetectorMultipleInterfaces) Addrs(intf *net.Interface)
 
 	if intf.Name == "eth0" {
 		_, ipnet1, _ := net.ParseCIDR("100.64.0.11/10")
-		_, ipnet2, _ := net.ParseCIDR("2005:DB6::/48")
-		return []net.Addr{ipnet1, ipnet2}, nil
+		_, ipnet2, _ := net.ParseCIDR("2001:0db8:85a3:0000:0000:8a2e:0370:7334/64")
+		ipAddr, _ := net.ResolveIPAddr("ip6", "fe80::140c:9579:8037:f565")
+		return []net.Addr{ipnet1, ipnet2, ipAddr}, nil
 	}
 
 	if intf.Name == "eth1" {
@@ -307,4 +308,16 @@ func TestNetworkFingerPrint_excludelo_down_interfaces(t *testing.T) {
 	if net.MBits == 0 {
 		t.Fatal("Expected Network Resource to have a non-zero bandwith")
 	}
+
+	// Test the CIDR of the IPs
+	if node.Resources.Networks[0].CIDR != "100.64.0.0/32" {
+		t.Fatalf("bad CIDR: %v", node.Resources.Networks[0].CIDR)
+	}
+	if node.Resources.Networks[1].CIDR != "2001:db8:85a3::/128" {
+		t.Fatalf("bad CIDR: %v", node.Resources.Networks[1].CIDR)
+	}
+	// Ensure that the link local address isn't fingerprinted
+	if len(node.Resources.Networks) != 2 {
+		t.Fatalf("bad number of IPs %v", len(node.Resources.Networks))
+	}
 }
diff --git a/website/source/docs/agent/configuration/client.html.md b/website/source/docs/agent/configuration/client.html.md
index 38cf283175e..d622f843c82 100644
--- a/website/source/docs/agent/configuration/client.html.md
+++ b/website/source/docs/agent/configuration/client.html.md
@@ -51,7 +51,9 @@ client {
 
 - `network_interface` `(string: "lo | lo0")` - Specifies the name of the
   interface to force network fingerprinting on. This defaults to the loopback
-  interface.
+  interface. All addresses on the interface are fingerprinted except the ones
+  which are scoped local for IPv6. The scheduler is going to pick one of the
+  many addresses which have been fingerprinted.
 
 - `network_speed` `(int: 0)` - Specifies an override for the network link speed.
   This value, if set, overrides any detected or defaulted link speed. Most