diff --git a/.changelog/13621.txt b/.changelog/13621.txt
new file mode 100644
index 000000000..acdffdf07
--- /dev/null
+++ b/.changelog/13621.txt
@@ -0,0 +1,3 @@
+```release-note:improvement
+api: HTTP server now returns a 429 error code when hitting the connection limit
+```
diff --git a/command/agent/http.go b/command/agent/http.go
index 2df2a6ac4..b0676ec82 100644
--- a/command/agent/http.go
+++ b/command/agent/http.go
@@ -14,6 +14,7 @@ import (
 	"strings"
 	"time"
 
+	"github.com/armon/go-metrics"
 	assetfs "github.com/elazarl/go-bindata-assetfs"
 	"github.com/gorilla/handlers"
 	"github.com/gorilla/websocket"
@@ -22,6 +23,7 @@ import (
 	"github.com/hashicorp/go-msgpack/codec"
 	multierror "github.com/hashicorp/go-multierror"
 	"github.com/rs/cors"
+	"golang.org/x/time/rate"
 
 	"github.com/hashicorp/nomad/acl"
 	"github.com/hashicorp/nomad/helper/noxssrw"
@@ -156,7 +158,7 @@ func NewHTTPServers(agent *Agent, config *Config) ([]*HTTPServer, error) {
 		httpServer := http.Server{
 			Addr:      srv.Addr,
 			Handler:   handlers.CompressHandler(srv.mux),
-			ConnState: makeConnState(config.TLSConfig.EnableHTTP, handshakeTimeout, maxConns),
+			ConnState: makeConnState(config.TLSConfig.EnableHTTP, handshakeTimeout, maxConns, srv.logger),
 			ErrorLog:  newHTTPServerLogger(srv.logger),
 		}
 
@@ -213,13 +215,12 @@ func NewHTTPServers(agent *Agent, config *Config) ([]*HTTPServer, error) {
 //
 // If limit > 0, a per-address connection limit will be enabled regardless of
 // TLS. If connLimit == 0 there is no connection limit.
-func makeConnState(isTLS bool, handshakeTimeout time.Duration, connLimit int) func(conn net.Conn, state http.ConnState) {
+func makeConnState(isTLS bool, handshakeTimeout time.Duration, connLimit int, logger log.Logger) func(conn net.Conn, state http.ConnState) {
+	connLimiter := connLimiter(connLimit, logger)
 	if !isTLS || handshakeTimeout == 0 {
 		if connLimit > 0 {
 			// Still return the connection limiter
-			return connlimit.NewLimiter(connlimit.Config{
-				MaxConnsPerClientIP: connLimit,
-			}).HTTPConnStateFunc()
+			return connLimiter
 		}
 		return nil
 	}
@@ -227,9 +228,6 @@ func makeConnState(isTLS bool, handshakeTimeout time.Duration, connLimit int) fu
 	if connLimit > 0 {
 		// Return conn state callback with connection limiting and a
 		// handshake timeout.
-		connLimiter := connlimit.NewLimiter(connlimit.Config{
-			MaxConnsPerClientIP: connLimit,
-		}).HTTPConnStateFunc()
 
 		return func(conn net.Conn, state http.ConnState) {
 			switch state {
@@ -268,6 +266,35 @@ func makeConnState(isTLS bool, handshakeTimeout time.Duration, connLimit int) fu
 	}
 }
 
+// connLimiter returns a connection-limiter function with a rate-limited 429-response error handler.
+// The rate-limit prevents the TLS handshake necessary to write the HTTP response
+// from consuming too many server resources.
+func connLimiter(connLimit int, logger log.Logger) func(conn net.Conn, state http.ConnState) {
+	// Global rate-limit of 10 responses per second with a 100-response burst.
+	limiter := rate.NewLimiter(10, 100)
+
+	tooManyConnsMsg := "Your IP is issuing too many concurrent connections, please rate limit your calls\n"
+	tooManyRequestsResponse := []byte(fmt.Sprintf("HTTP/1.1 429 Too Many Requests\r\n"+
+		"Content-Type: text/plain\r\n"+
+		"Content-Length: %d\r\n"+
+		"Connection: close\r\n\r\n%s", len(tooManyConnsMsg), tooManyConnsMsg))
+	return connlimit.NewLimiter(connlimit.Config{
+		MaxConnsPerClientIP: connLimit,
+	}).HTTPConnStateFuncWithErrorHandler(func(err error, conn net.Conn) {
+		if err == connlimit.ErrPerClientIPLimitReached {
+			metrics.IncrCounter([]string{"nomad", "agent", "http", "exceeded"}, 1)
+			if n := limiter.Reserve(); n.Delay() == 0 {
+				logger.Warn("Too many concurrent connections", "address", conn.RemoteAddr().String(), "limit", connLimit)
+				conn.SetDeadline(time.Now().Add(10 * time.Millisecond))
+				conn.Write(tooManyRequestsResponse)
+			} else {
+				n.Cancel()
+			}
+		}
+		conn.Close()
+	})
+}
+
 // tcpKeepAliveListener sets TCP keep-alive timeouts on accepted
 // connections. It's used by NewHttpServer so
 // dead TCP connections eventually go away.
diff --git a/command/agent/http_test.go b/command/agent/http_test.go
index 5c817c308..7beb8f080 100644
--- a/command/agent/http_test.go
+++ b/command/agent/http_test.go
@@ -1254,41 +1254,15 @@ func TestHTTPServer_Limits_OK(t *testing.T) {
 		// Create a new connection that will go over the connection limit.
 		limitConn, err := dial(t, addr, useTLS)
 
-		// At this point, the state of the connection + handshake are up in the
-		// air.
-		//
-		// 1) dial failed, handshake never started
-		//     => Conn is nil + io.EOF
-		// 2) dial completed, handshake failed
-		//     => Conn is malformed + (net.OpError OR io.EOF)
-		// 3) dial completed, handshake succeeded
-		//     => Conn is not nil + no error, however using the Conn should
-		//        result in io.EOF
-		//
-		// At no point should Nomad actually write through the limited Conn.
-
-		if limitConn == nil || err != nil {
-			// Case 1 or Case 2 - returned Conn is useless and the error should
-			// be one of:
-			//   "EOF"
-			//   "closed network connection"
-			//   "connection reset by peer"
-			msg := err.Error()
-			acceptable := strings.Contains(msg, "EOF") ||
-				strings.Contains(msg, "closed network connection") ||
-				strings.Contains(msg, "connection reset by peer")
-			require.True(t, acceptable)
-		} else {
-			// Case 3 - returned Conn is usable, but Nomad should not write
-			// anything before closing it.
-			buf := make([]byte, bufSize)
-			deadline := time.Now().Add(10 * time.Second)
-			require.NoError(t, limitConn.SetReadDeadline(deadline))
-			n, err := limitConn.Read(buf)
-			require.Equal(t, io.EOF, err)
-			require.Zero(t, n)
-			require.NoError(t, limitConn.Close())
-		}
+		response := "HTTP/1.1 429"
+		buf := make([]byte, len(response))
+		deadline := time.Now().Add(10 * time.Second)
+		require.NoError(t, limitConn.SetReadDeadline(deadline))
+		n, err := limitConn.Read(buf)
+		require.Equal(t, response, string(buf))
+		require.Nil(t, err)
+		require.Equal(t, len(response), n)
+		require.NoError(t, limitConn.Close())
 
 		// Assert existing connections are ok
 		require.Len(t, errCh, 0)
diff --git a/website/content/docs/operations/metrics-reference.mdx b/website/content/docs/operations/metrics-reference.mdx
index 434d5690f..125ba4484 100644
--- a/website/content/docs/operations/metrics-reference.mdx
+++ b/website/content/docs/operations/metrics-reference.mdx
@@ -480,6 +480,14 @@ Raft database metrics are emitted by the `raft-boltdb` library.
 | `nomad.raft.boltdb.txstats.write`         | Count of total write operations           | Integer     | Counter |
 | `nomad.raft.boltdb.txstats.writeTime`     | Sample of write operation times           | Nanoseconds | Summary |
 
+## Agent Metrics
+
+Agent metrics are emitted by all Nomad agents running in either client or server mode.
+
+| Metric                                    | Description                                           | Unit        | Type    |
+| ----------------------------------------- | ----------------------------------------------------- | ----------- | ------- |
+| `nomad.agent.http.exceeded`               | Count of HTTP connections exceeding concurrency limit | Integer     | Counter |
+
 [tagged-metrics]: /docs/telemetry/metrics#tagged-metrics
 [sticky]: /docs/job-specification/ephemeral_disk#sticky
 [s_port_plan_failure]: /s/port-plan-failure