diff --git a/CHANGELOG.md b/CHANGELOG.md
index 40bf6efed..d26c00e2c 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -203,6 +203,7 @@
   * `gate_duration_seconds`
   * `kv_request_duration_seconds`
   * `operation_duration_seconds`
+* [ENHANCEMENT] Implement UNIX socket support for gRPC and HTTP listeners. #511
 * [BUGFIX] spanlogger: Support multiple tenant IDs. #59
 * [BUGFIX] Memberlist: fixed corrupted packets when sending compound messages with more than 255 messages or messages bigger than 64KB. #85
 * [BUGFIX] Ring: `ring_member_ownership_percent` and `ring_tokens_owned` metrics are not updated on scale down. #109
diff --git a/server/server.go b/server/server.go
index c39e3873c..71843fe96 100644
--- a/server/server.go
+++ b/server/server.go
@@ -48,6 +48,8 @@ const (
 	DefaultNetwork = "tcp"
 	// NetworkTCPV4 for IPV4 only
 	NetworkTCPV4 = "tcp4"
+	// NetworkUnix for UNIX sockets
+	NetworkUnix = "unix"
 )
 
 // SignalHandler used by Server.
@@ -263,8 +265,16 @@ func newServer(cfg Config, metrics *Metrics) (*Server, error) {
 	if network == "" {
 		network = DefaultNetwork
 	}
+
+	// Generate a listen address depending on the configured network.
+	httpListenAddr := net.JoinHostPort(cfg.HTTPListenAddress, strconv.Itoa(cfg.HTTPListenPort))
+	if network == "unix" {
+		// If we're using unix sockets instead of a TCP socket, don't set a port.
+		httpListenAddr = cfg.HTTPListenAddress
+	}
+
 	// Setup listeners first, so we can fail early if the port is in use.
-	httpListener, err := net.Listen(network, net.JoinHostPort(cfg.HTTPListenAddress, strconv.Itoa(cfg.HTTPListenPort)))
+	httpListener, err := net.Listen(network, httpListenAddr)
 	if err != nil {
 		return nil, err
 	}
@@ -282,7 +292,15 @@ func newServer(cfg Config, metrics *Metrics) (*Server, error) {
 	if network == "" {
 		network = DefaultNetwork
 	}
-	grpcListener, err := net.Listen(network, net.JoinHostPort(cfg.GRPCListenAddress, strconv.Itoa(cfg.GRPCListenPort)))
+
+	// Generate a listen address depending on the configured network.
+	grpcListenAddr := net.JoinHostPort(cfg.GRPCListenAddress, strconv.Itoa(cfg.GRPCListenPort))
+	if network == "unix" {
+		// If we're using unix sockets instead of a TCP socket, don't set a port.
+		grpcListenAddr = cfg.GRPCListenAddress
+	}
+
+	grpcListener, err := net.Listen(network, grpcListenAddr)
 	if err != nil {
 		return nil, err
 	}
diff --git a/server/server_test.go b/server/server_test.go
index b15f4da26..74b1d01cf 100644
--- a/server/server_test.go
+++ b/server/server_test.go
@@ -128,6 +128,53 @@ func TestTCPv4Network(t *testing.T) {
 	})
 }
 
+func TestUnixNetwork(t *testing.T) {
+	testSockDir, err := os.MkdirTemp("", "sock")
+	require.NoError(t, err)
+	t.Cleanup(func() {
+		require.NoError(t, os.RemoveAll(testSockDir))
+	})
+
+	var cfg Config
+	setAutoAssignedPorts(NetworkUnix, &cfg)
+	cfg.HTTPListenAddress = filepath.Join(testSockDir, "http.sock")
+	cfg.GRPCListenAddress = filepath.Join(testSockDir, "grpc.sock")
+
+	t.Run("unix_http", func(t *testing.T) {
+		var level log.Level
+		require.NoError(t, level.Set("info"))
+		cfg.LogLevel = level
+		cfg.MetricsNamespace = "testing_http_unix"
+		srv, err := New(cfg)
+		require.NoError(t, err)
+
+		errChan := make(chan error, 1)
+		go func() {
+			errChan <- srv.Run()
+		}()
+
+		require.NoError(t, srv.httpListener.Close())
+		require.NotNil(t, <-errChan)
+
+		// So that address is freed for further tests.
+		srv.GRPC.Stop()
+	})
+
+	t.Run("unix_http", func(t *testing.T) {
+		cfg.MetricsNamespace = "testing_grpc_unix"
+		srv, err := New(cfg)
+		require.NoError(t, err)
+
+		errChan := make(chan error, 1)
+		go func() {
+			errChan <- srv.Run()
+		}()
+
+		require.NoError(t, srv.grpcListener.Close())
+		require.NotNil(t, <-errChan)
+	})
+}
+
 // Ensure that http and grpc servers work with no overrides to config
 // (except http port because an ordinary user can't bind to default port 80)
 func TestDefaultAddresses(t *testing.T) {