diff --git a/api/utils/route.go b/api/utils/route.go
index 476b53f177511..a34ccc00d5c76 100644
--- a/api/utils/route.go
+++ b/api/utils/route.go
@@ -18,6 +18,7 @@ import (
 	"context"
 	"errors"
 	"net"
+	"strings"
 	"unicode/utf8"
 
 	"github.com/google/uuid"
@@ -49,6 +50,8 @@ type SSHRouteMatcherConfig struct {
 	Resolver HostResolver
 	// CaseInsensitive enabled case insensitive routing when true.
 	CaseInsensitive bool
+	// DisableUnqualifiedLookups disables lookups for unqualified hostnames.
+	DisableUnqualifiedLookups bool
 }
 
 // HostResolver provides an interface matching the net.Resolver.LookupHost method. Typically
@@ -88,7 +91,12 @@ func newSSHRouteMatcher(cfg SSHRouteMatcherConfig) SSHRouteMatcher {
 	_, err := uuid.Parse(cfg.Host)
 	dialByID := err == nil || aws.IsEC2NodeID(cfg.Host)
 
-	ips, _ := cfg.Resolver.LookupHost(context.Background(), cfg.Host)
+	var ips []string
+	if !(cfg.DisableUnqualifiedLookups && !strings.Contains(cfg.Host, ".")) {
+		// unqualified lookups are still on by default, but future versions of teleport may disable them as they tend
+		// to be responsible for the majority of all lookups generated by a teleport cluster and are of questionable utility.
+		ips, _ = cfg.Resolver.LookupHost(context.Background(), cfg.Host)
+	}
 
 	return SSHRouteMatcher{
 		cfg:            cfg,
diff --git a/api/utils/route_test.go b/api/utils/route_test.go
index 5de05efa673d8..ce971e04e6ea3 100644
--- a/api/utils/route_test.go
+++ b/api/utils/route_test.go
@@ -323,3 +323,66 @@ func TestSSHRouteMatcherScoring(t *testing.T) {
 		})
 	}
 }
+
+type recordingHostResolver struct {
+	didLookup bool
+}
+
+func (r *recordingHostResolver) LookupHost(ctx context.Context, host string) (addrs []string, err error) {
+	r.didLookup = true
+	return nil, nil
+}
+
+// TestDisableUnqualifiedLookups verifies that unqualified lookups being disabled results
+// in single-element/tld style hostname targets not being resolved.
+func TestDisableUnqualifiedLookups(t *testing.T) {
+	tts := []struct {
+		desc   string
+		target string
+		lookup bool
+	}{
+		{
+			desc:   "qualified hostname",
+			target: "example.com",
+			lookup: true,
+		},
+		{
+			desc:   "unqualified hostname",
+			target: "example",
+			lookup: false,
+		},
+		{
+			desc:   "localhost",
+			target: "localhost",
+			lookup: false,
+		},
+		{
+			desc:   "foo.localhost",
+			target: "foo.localhost",
+			lookup: true,
+		},
+		{
+			desc:   "uuid",
+			target: uuid.NewString(),
+			lookup: false,
+		},
+		{
+			desc:   "qualified uuid",
+			target: "foo." + uuid.NewString(),
+			lookup: true,
+		},
+	}
+
+	for _, tt := range tts {
+		t.Run(tt.desc, func(t *testing.T) {
+			resolver := &recordingHostResolver{}
+			_, err := NewSSHRouteMatcherFromConfig(SSHRouteMatcherConfig{
+				Host:                      tt.target,
+				Resolver:                  resolver,
+				DisableUnqualifiedLookups: true,
+			})
+			require.NoError(t, err)
+			require.Equal(t, tt.lookup, resolver.didLookup)
+		})
+	}
+}
diff --git a/lib/auth/auth_with_roles.go b/lib/auth/auth_with_roles.go
index 572b920e16d33..1749c94bb4402 100644
--- a/lib/auth/auth_with_roles.go
+++ b/lib/auth/auth_with_roles.go
@@ -20,6 +20,7 @@ import (
 	"context"
 	"fmt"
 	"net/url"
+	"os"
 	"slices"
 	"strings"
 	"time"
@@ -1763,6 +1764,8 @@ func (a *ServerWithRoles) authContextForSearch(ctx context.Context, req *proto.L
 	return extendedContext, nil
 }
 
+var disableUnqualifiedLookups = os.Getenv("TELEPORT_UNSTABLE_DISABLE_UNQUALIFIED_LOOKUPS") == "yes"
+
 // GetSSHTargets gets all servers that would match an equivalent ssh dial request. Note that this method
 // returns all resources directly accessible to the user *and* all resources available via 'SearchAsRoles',
 // which is what we want when handling things like ambiguous host errors and resource-based access requests,
@@ -1775,7 +1778,15 @@ func (a *ServerWithRoles) GetSSHTargets(ctx context.Context, req *proto.GetSSHTa
 		caseInsensitiveRouting = cfg.GetCaseInsensitiveRouting()
 	}
 
-	matcher := apiutils.NewSSHRouteMatcher(req.Host, req.Port, caseInsensitiveRouting)
+	matcher, err := apiutils.NewSSHRouteMatcherFromConfig(apiutils.SSHRouteMatcherConfig{
+		Host:                      req.Host,
+		Port:                      req.Port,
+		CaseInsensitive:           caseInsensitiveRouting,
+		DisableUnqualifiedLookups: disableUnqualifiedLookups,
+	})
+	if err != nil {
+		return nil, trace.Wrap(err)
+	}
 
 	lreq := proto.ListResourcesRequest{
 		ResourceType:     types.KindNode,
diff --git a/lib/proxy/router.go b/lib/proxy/router.go
index 3e1ba64361149..fc9d503cbbb3e 100644
--- a/lib/proxy/router.go
+++ b/lib/proxy/router.go
@@ -448,6 +448,8 @@ func getServer(ctx context.Context, host, port string, site site) (types.Server,
 	return getServerWithResolver(ctx, host, port, site, nil /* use default resolver */)
 }
 
+var disableUnqualifiedLookups = os.Getenv("TELEPORT_UNSTABLE_DISABLE_UNQUALIFIED_LOOKUPS") == "yes"
+
 // getServerWithResolver attempts to locate a node matching the provided host and port in
 // the provided site. The resolver argument is used in certain tests to mock DNS resolution
 // and can generally be left nil.
@@ -464,10 +466,11 @@ func getServerWithResolver(ctx context.Context, host, port string, site site, re
 	}
 
 	routeMatcher, err := apiutils.NewSSHRouteMatcherFromConfig(apiutils.SSHRouteMatcherConfig{
-		Host:            host,
-		Port:            port,
-		CaseInsensitive: caseInsensitiveRouting,
-		Resolver:        resolver,
+		Host:                      host,
+		Port:                      port,
+		CaseInsensitive:           caseInsensitiveRouting,
+		Resolver:                  resolver,
+		DisableUnqualifiedLookups: disableUnqualifiedLookups,
 	})
 	if err != nil {
 		return nil, trace.Wrap(err)