diff --git a/hscontrol/noise.go b/hscontrol/noise.go
index cced5e1c2..4ca7e0f7e 100644
--- a/hscontrol/noise.go
+++ b/hscontrol/noise.go
@@ -430,6 +430,7 @@ func (ns *noiseServer) SSHActionHandler(
 		req.Context(),
 		reqLog,
 		srcNodeID, dstNodeID,
+		req.URL.Query().Get("local_user"),
 		req.URL.Query().Get("auth_id"),
 	)
 	if err != nil {
@@ -470,7 +471,7 @@ func (ns *noiseServer) sshAction(
 	ctx context.Context,
 	reqLog zerolog.Logger,
 	srcNodeID, dstNodeID types.NodeID,
-	authIDStr string,
+	localUser, authIDStr string,
 ) (*tailcfg.SSHAction, error) {
 	action := tailcfg.SSHAction{
 		AllowAgentForwarding:      true,
@@ -480,8 +481,10 @@ func (ns *noiseServer) sshAction(
 
 	// Look up check params from the server's own policy rather than
 	// trusting URL parameters, which the client could tamper with.
+	// local_user only narrows which rule applies, and it comes from dst,
+	// the node enforcing the login.
 	checkPeriod, checkFound := ns.headscale.state.SSHCheckParams(
-		srcNodeID, dstNodeID,
+		srcNodeID, dstNodeID, localUser,
 	)
 
 	// Clients only call back for check rules they were sent. Without one in
@@ -494,7 +497,7 @@ func (ns *noiseServer) sshAction(
 	if authIDStr != "" {
 		return ns.sshActionFollowUp(
 			ctx, reqLog, &action, authIDStr,
-			srcNodeID, dstNodeID,
+			srcNodeID, dstNodeID, localUser,
 		)
 	}
 
@@ -515,7 +518,7 @@ func (ns *noiseServer) sshAction(
 	}
 
 	// No auto-approval — create an auth session and hold.
-	return ns.sshActionHoldAndDelegate(reqLog, &action, srcNodeID, dstNodeID)
+	return ns.sshActionHoldAndDelegate(reqLog, &action, srcNodeID, dstNodeID, localUser)
 }
 
 // sshActionDeny rejects a check the current policy does not require. It is a
@@ -536,11 +539,11 @@ func (ns *noiseServer) sshActionHoldAndDelegate(
 	reqLog zerolog.Logger,
 	action *tailcfg.SSHAction,
 	srcNodeID, dstNodeID types.NodeID,
+	localUser string,
 ) (*tailcfg.SSHAction, error) {
 	holdURL, err := url.Parse(
 		ns.headscale.cfg.ServerURL +
-			"/machine/ssh/action/$SRC_NODE_ID/to/$DST_NODE_ID" +
-			"?local_user=$LOCAL_USER",
+			"/machine/ssh/action/$SRC_NODE_ID/to/$DST_NODE_ID",
 	)
 	if err != nil {
 		return nil, NewHTTPError(
@@ -566,7 +569,10 @@ func (ns *noiseServer) sshActionHoldAndDelegate(
 
 	authURL := ns.headscale.authProvider.AuthURL(authID)
 
+	// The concrete user, not $LOCAL_USER: Encode escapes the placeholder
+	// and tailssh only expands it literally.
 	q := holdURL.Query()
+	q.Set("local_user", localUser)
 	q.Set("auth_id", authID.String())
 	holdURL.RawQuery = q.Encode()
 
@@ -597,6 +603,7 @@ func (ns *noiseServer) sshActionFollowUp(
 	action *tailcfg.SSHAction,
 	authIDStr string,
 	srcNodeID, dstNodeID types.NodeID,
+	localUser string,
 ) (*tailcfg.SSHAction, error) {
 	authID, err := types.AuthIDFromString(authIDStr)
 	if err != nil {
@@ -616,7 +623,7 @@ func (ns *noiseServer) sshActionFollowUp(
 		reqLog.Info().Caller().Msg(logMsg)
 
 		return ns.sshActionHoldAndDelegate(
-			reqLog, action, srcNodeID, dstNodeID,
+			reqLog, action, srcNodeID, dstNodeID, localUser,
 		)
 	}
 
@@ -691,7 +698,7 @@ func (ns *noiseServer) sshActionFollowUp(
 
 	// The policy may have changed while the user authenticated, and the
 	// client won't drop a connection still waiting on its check.
-	if _, ok := ns.headscale.state.SSHCheckParams(srcNodeID, dstNodeID); !ok {
+	if _, ok := ns.headscale.state.SSHCheckParams(srcNodeID, dstNodeID, localUser); !ok {
 		return sshActionDeny(reqLog, action), nil
 	}
 
diff --git a/hscontrol/noise_test.go b/hscontrol/noise_test.go
index 3ec37ea89..dcaf40969 100644
--- a/hscontrol/noise_test.go
+++ b/hscontrol/noise_test.go
@@ -14,6 +14,7 @@ import (
 	"slices"
 	"strconv"
 	"sync"
+	"strings"
 	"testing"
 	"time"
 
@@ -448,13 +449,17 @@ func TestSSHActionRoute_OldPathReturns404(t *testing.T) {
 	}
 }
 
+// sshTestLocalUser is the non-root local user the SSH action tests log in as.
+const sshTestLocalUser = "alice"
+
 // newSSHActionRequest builds an httptest request with the chi URL params
 // [noiseServer.SSHActionHandler] reads (src_node_id and dst_node_id), so the handler
 // can be exercised directly without going through the chi router.
 func newSSHActionRequest(t *testing.T, src, dst types.NodeID) *http.Request {
 	t.Helper()
 
-	url := fmt.Sprintf("/machine/ssh/action/%d/to/%d", src.Uint64(), dst.Uint64())
+	url := fmt.Sprintf("/machine/ssh/action/%d/to/%d?local_user=%s",
+		src.Uint64(), dst.Uint64(), sshTestLocalUser)
 	req := httptest.NewRequestWithContext(context.Background(), http.MethodGet, url, nil)
 
 	rctx := chi.NewRouteContext()
@@ -510,7 +515,7 @@ func putSSHCheckNodes(t *testing.T, app *Headscale, userName string, hostnames .
 	_, err := app.state.SetPolicy([]byte(sshCheckPolicy(userName)))
 	require.NoError(t, err)
 
-	_, checkFound := app.state.SSHCheckParams(nodes[0].ID, nodes[len(nodes)-1].ID)
+	_, checkFound := app.state.SSHCheckParams(nodes[0].ID, nodes[len(nodes)-1].ID, sshTestLocalUser)
 	require.True(t, checkFound, "test setup: nodes must be subject to an SSH check")
 
 	return nodes
@@ -601,8 +606,8 @@ func TestSSHActionFollowUp_RejectsBindingMismatch(t *testing.T) {
 	}
 
 	url := fmt.Sprintf(
-		"/machine/ssh/action/%d/to/%d?auth_id=%s",
-		srcOther.ID.Uint64(), dstOther.ID.Uint64(), authID.String(),
+		"/machine/ssh/action/%d/to/%d?local_user=%s&auth_id=%s",
+		srcOther.ID.Uint64(), dstOther.ID.Uint64(), sshTestLocalUser, authID.String(),
 	)
 	req := httptest.NewRequestWithContext(context.Background(), http.MethodGet, url, nil)
 
@@ -693,7 +698,7 @@ func TestSSHActionHandler_RejectsWithoutCheck(t *testing.T) {
 	src := putTestNodeInStore(t, app, user, "src-node")
 	dst := putTestNodeInStore(t, app, user, "dst-node")
 
-	_, checkFound := app.state.SSHCheckParams(src.ID, dst.ID)
+	_, checkFound := app.state.SSHCheckParams(src.ID, dst.ID, sshTestLocalUser)
 	require.False(t, checkFound, "test setup: pair must not be subject to a check")
 
 	ns := &noiseServer{headscale: app, machineKey: dst.MachineKey}
@@ -720,17 +725,31 @@ func TestSSHActionHandler_RejectsWithoutCheck(t *testing.T) {
 func TestSSHActionFollowUp_RejectsVerdictAfterCheckRemoved(t *testing.T) {
 	t.Parallel()
 
-	for name, removeRule := range map[string]bool{
-		"rule kept":    false,
-		"rule removed": true,
+	const userName = "ssh-verdict-user"
+
+	nonrootOnly := sshCheckPolicy(userName)
+	rootAndNonroot := strings.Replace(nonrootOnly,
+		`["autogroup:nonroot"]`, `["root", "autogroup:nonroot"]`, 1)
+
+	for name, tc := range map[string]struct {
+		after     string // policy once the user has authenticated; "" keeps it
+		localUser string
+	}{
+		"rule kept":    {"", sshTestLocalUser},
+		"rule removed": {`{}`, sshTestLocalUser},
+		// Another check rule still covers the pair, but not for root.
+		"root rule removed": {nonrootOnly, "root"},
 	} {
 		t.Run(name, func(t *testing.T) {
 			t.Parallel()
 
 			app := createTestApp(t)
-			nodes := putSSHCheckNodes(t, app, "ssh-verdict-user", "src-node", "dst-node")
+			nodes := putSSHCheckNodes(t, app, userName, "src-node", "dst-node")
 			src, dst := nodes[0], nodes[1]
 
+			_, err := app.state.SetPolicy([]byte(rootAndNonroot))
+			require.NoError(t, err)
+
 			authID := types.MustAuthID()
 			app.state.SetAuthCacheEntry(authID, types.NewSSHCheckAuthRequest(src.ID, dst.ID))
 
@@ -738,8 +757,8 @@ func TestSSHActionFollowUp_RejectsVerdictAfterCheckRemoved(t *testing.T) {
 			require.True(t, ok)
 			auth.FinishAuth(types.AuthVerdict{})
 
-			if removeRule {
-				_, err := app.state.SetPolicy([]byte(`{}`))
+			if tc.after != "" {
+				_, err := app.state.SetPolicy([]byte(tc.after))
 				require.NoError(t, err)
 			}
 
@@ -749,15 +768,16 @@ func TestSSHActionFollowUp_RejectsVerdictAfterCheckRemoved(t *testing.T) {
 			// the policy changed while the user was authenticating.
 			action, err := ns.sshActionFollowUp(
 				t.Context(), zerolog.Nop(), &tailcfg.SSHAction{},
-				authID.String(), src.ID, dst.ID,
+				authID.String(), src.ID, dst.ID, tc.localUser,
 			)
 			require.NoError(t, err)
 
+			kept := tc.after == ""
 			_, recorded := app.state.GetLastSSHAuth(src.ID, dst.ID)
 
-			assert.Equal(t, !removeRule, action.Accept, "accept, got %+v", action)
-			assert.Equal(t, removeRule, action.Reject, "reject, got %+v", action)
-			assert.Equal(t, !removeRule, recorded, "auth recorded for auto-approval")
+			assert.Equal(t, kept, action.Accept, "accept, got %+v", action)
+			assert.Equal(t, !kept, action.Reject, "reject, got %+v", action)
+			assert.Equal(t, kept, recorded, "auth recorded for auto-approval")
 		})
 	}
 }
diff --git a/hscontrol/policy/pm.go b/hscontrol/policy/pm.go
index 78bf62438..ba8a61051 100644
--- a/hscontrol/policy/pm.go
+++ b/hscontrol/policy/pm.go
@@ -21,9 +21,10 @@ type PolicyManager interface {
 	// BuildPeerMap constructs peer relationship maps for the given nodes
 	BuildPeerMap(nodes views.Slice[types.NodeView]) map[types.NodeID][]types.NodeID
 	SSHPolicy(baseURL string, node types.NodeView) (*tailcfg.SSHPolicy, error)
-	// SSHCheckParams resolves the SSH check period for a (src, dst) pair
-	// from the current policy, avoiding trust of client-provided URL params.
-	SSHCheckParams(srcNodeID, dstNodeID types.NodeID) (time.Duration, bool)
+	// SSHCheckParams resolves the SSH check period for src logging in to
+	// dst as localUser from the current policy, avoiding trust of
+	// client-provided URL params.
+	SSHCheckParams(srcNodeID, dstNodeID types.NodeID, localUser string) (time.Duration, bool)
 	SetPolicy(pol []byte) (bool, error)
 	// SetUsers replaces the user list. policyChanged reports whether clients
 	// need a policy refresh; peerMapChanged reports whether user-derived peer
diff --git a/hscontrol/policy/v2/filter_test.go b/hscontrol/policy/v2/filter_test.go
index 80cbe0ce5..fcdb7e66e 100644
--- a/hscontrol/policy/v2/filter_test.go
+++ b/hscontrol/policy/v2/filter_test.go
@@ -2753,11 +2753,35 @@ func TestIPSetToPrincipals(t *testing.T) {
 	}
 }
 
+// overlappingSSHChecks has a localpart check rule whose self-access reaches
+// user1's own nodes ahead of an always-check root rule for the same pair.
+var overlappingSSHChecks = []byte(`{
+	"tagOwners": {"tag:server": ["user1@"]},
+	"ssh": [
+		{
+			"action": "check",
+			"checkPeriod": "12h",
+			"src": ["user1@"],
+			"dst": ["tag:server"],
+			"users": ["localpart:*@example.com"]
+		},
+		{
+			"action": "check",
+			"checkPeriod": "always",
+			"src": ["user1@"],
+			"dst": ["autogroup:self"],
+			"users": ["root"]
+		}
+	]
+}`)
+
 func TestSSHCheckParams(t *testing.T) {
 	users := types.Users{
 		{Name: "user1", ID: 1},
 		{Name: "user2", ID: 2},
 	}
+	users[0].Email = "user1@example.com"
+	users[1].Email = "user2@example.com"
 
 	nodeUser1 := types.Node{
 		ID:       1,
@@ -2789,6 +2813,7 @@ func TestSSHCheckParams(t *testing.T) {
 		policy     []byte
 		srcID      types.NodeID
 		dstID      types.NodeID
+		localUser  string // defaults to a non-root user
 		wantPeriod time.Duration
 		wantOK     bool
 	}{
@@ -2936,6 +2961,66 @@ func TestSSHCheckParams(t *testing.T) {
 			dstID:  types.NodeID(2),
 			wantOK: false,
 		},
+		{
+			name: "root rejected by a nonroot rule",
+			policy: []byte(`{
+				"tagOwners": {"tag:server": ["user1@"]},
+				"ssh": [{
+					"action": "check",
+					"src": ["user2@"],
+					"dst": ["tag:server"],
+					"users": ["autogroup:nonroot"]
+				}]
+			}`),
+			srcID:     types.NodeID(2),
+			dstID:     types.NodeID(3),
+			localUser: "root",
+			wantOK:    false,
+		},
+		{
+			name: "literal user must match",
+			policy: []byte(`{
+				"tagOwners": {"tag:server": ["user1@"]},
+				"ssh": [{
+					"action": "check",
+					"src": ["user2@"],
+					"dst": ["tag:server"],
+					"users": ["deploy"]
+				}]
+			}`),
+			srcID:     types.NodeID(2),
+			dstID:     types.NodeID(3),
+			localUser: "other",
+			wantOK:    false,
+		},
+		{
+			// The client skips the localpart rule for root and enforces
+			// the later always-check root rule; so must the server.
+			name:       "overlapping rules: root skips localpart self-access",
+			policy:     overlappingSSHChecks,
+			srcID:      types.NodeID(1),
+			dstID:      types.NodeID(1),
+			localUser:  "root",
+			wantPeriod: 0,
+			wantOK:     true,
+		},
+		{
+			name:       "overlapping rules: localpart user gets its period",
+			policy:     overlappingSSHChecks,
+			srcID:      types.NodeID(1),
+			dstID:      types.NodeID(1),
+			localUser:  "user1",
+			wantPeriod: 12 * time.Hour,
+			wantOK:     true,
+		},
+		{
+			name:      "overlapping rules: another user's localpart is rejected",
+			policy:    overlappingSSHChecks,
+			srcID:     types.NodeID(1),
+			dstID:     types.NodeID(1),
+			localUser: "user2",
+			wantOK:    false,
+		},
 	}
 
 	for _, tt := range tests {
@@ -2943,7 +3028,12 @@ func TestSSHCheckParams(t *testing.T) {
 			pm, err := NewPolicyManager(tt.policy, users, nodes.ViewSlice())
 			require.NoError(t, err)
 
-			period, ok := pm.SSHCheckParams(tt.srcID, tt.dstID)
+			localUser := tt.localUser
+			if localUser == "" {
+				localUser = "alice"
+			}
+
+			period, ok := pm.SSHCheckParams(tt.srcID, tt.dstID, localUser)
 			assert.Equal(t, tt.wantOK, ok, "ok mismatch")
 
 			if tt.wantOK {
diff --git a/hscontrol/policy/v2/policy.go b/hscontrol/policy/v2/policy.go
index 306e00151..ff4e2258c 100644
--- a/hscontrol/policy/v2/policy.go
+++ b/hscontrol/policy/v2/policy.go
@@ -477,16 +477,18 @@ func (pm *PolicyManager) SSHPolicy(baseURL string, node types.NodeView) (*tailcf
 	return sshPol, nil
 }
 
-// SSHCheckParams resolves the SSH check period for a source-destination
-// node pair by looking up the current policy. This avoids trusting URL
+// SSHCheckParams resolves the SSH check period for src logging in to dst
+// as localUser by looking up the current policy. This avoids trusting URL
 // parameters that a client could tamper with. First-match wins across
-// the policy's SSH rules.
+// the policy's SSH rules; a rule only matches when it lets src log in as
+// localUser, as the client does when it picks the rule.
 //
 // Returns (duration, true) when a matching rule is found and
 // (0, false) when none is. A (0, true) return means the matched rule
 // uses a zero check period (re-check every session).
 func (pm *PolicyManager) SSHCheckParams(
 	srcNodeID, dstNodeID types.NodeID,
+	localUser string,
 ) (time.Duration, bool) {
 	pm.mu.RLock()
 	defer pm.mu.RUnlock()
@@ -533,20 +535,16 @@ func (pm *PolicyManager) SSHCheckParams(
 			continue
 		}
 
+		if !pm.sshRuleAllowsUser(rule, srcNode, localUser) {
+			continue
+		}
+
 		// Check if dst node matches any destination.
 		hasOtherDests := false
 
 		for _, dst := range rule.Destinations {
 			if ag, isAG := dst.(*AutoGroup); isAG && ag.Is(AutoGroupSelf) {
-				// User().Valid() guards the User().ID() dereference: the
-				// NodeStore can hold a non-tagged node with UserID set but
-				// the User association unhydrated (nil), and IsTagged()
-				// alone does not cover that. Mirrors filter.go's
-				// autogroup:self guard. Without it, a tailnet client on the
-				// Noise SSH-check path crashes the server (nil deref).
-				if !srcNode.IsTagged() && !dstNode.IsTagged() &&
-					srcNode.User().Valid() && dstNode.User().Valid() &&
-					srcNode.User().ID() == dstNode.User().ID() {
+				if sshNodesShareUser(srcNode, dstNode) {
 					return checkPeriodFromRule(rule), true
 				}
 
@@ -573,9 +571,7 @@ func (pm *PolicyManager) SSHCheckParams(
 				if srcNodeID == dstNodeID {
 					return checkPeriodFromRule(rule), true
 				}
-			} else if !srcNode.IsTagged() &&
-				srcNode.User().Valid() && dstNode.User().Valid() &&
-				srcNode.User().ID() == dstNode.User().ID() {
+			} else if sshNodesShareUser(srcNode, dstNode) {
 				return checkPeriodFromRule(rule), true
 			}
 		}
@@ -584,6 +580,38 @@ func (pm *PolicyManager) SSHCheckParams(
 	return 0, false
 }
 
+// sshNodesShareUser matches user-owned nodes with hydrated user associations.
+// IsTagged alone does not guard User().ID(): the NodeStore can hold a
+// non-tagged node whose UserID is set but whose User association is nil.
+func sshNodesShareUser(srcNode, dstNode types.NodeView) bool {
+	return !srcNode.IsTagged() && !dstNode.IsTagged() &&
+		srcNode.User().Valid() && dstNode.User().Valid() &&
+		srcNode.User().ID() == dstNode.User().ID()
+}
+
+// sshRuleAllowsUser reports whether rule lets src log in as localUser,
+// mirroring the SSHUsers maps compileSSHPolicy emits: root when listed,
+// other users via autogroup:nonroot or a literal name, and anyone, root
+// included, whose name is the source user's localpart.
+func (pm *PolicyManager) sshRuleAllowsUser(rule SSH, srcNode types.NodeView, localUser string) bool {
+	isRoot := localUser == "root"
+
+	switch {
+	case localUser == "":
+		return false
+	case isRoot && rule.Users.ContainsRoot(),
+		!isRoot && rule.Users.ContainsNonRoot(),
+		!isRoot && slices.Contains(rule.Users.NormalUsers(), SSHUser(localUser)):
+		return true
+	case srcNode.IsTagged() || !srcNode.User().Valid() || !rule.Users.ContainsLocalpart():
+		return false
+	}
+
+	lp, ok := resolveLocalparts(rule.Users.LocalpartEntries(), pm.users)[srcNode.User().ID()]
+
+	return ok && lp == localUser
+}
+
 func (pm *PolicyManager) SetPolicy(polB []byte) (bool, error) {
 	if len(polB) == 0 {
 		return false, nil
diff --git a/hscontrol/policy/v2/policy_test.go b/hscontrol/policy/v2/policy_test.go
index 57720c7bb..c5a427ebf 100644
--- a/hscontrol/policy/v2/policy_test.go
+++ b/hscontrol/policy/v2/policy_test.go
@@ -392,7 +392,7 @@ func TestSSHCheckParamsUnhydratedUserNoPanic(t *testing.T) {
 	require.NoError(t, err)
 
 	require.NotPanics(t, func() {
-		pm.SSHCheckParams(types.NodeID(1), types.NodeID(2))
+		pm.SSHCheckParams(types.NodeID(1), types.NodeID(2), "alice")
 	}, "SSHCheckParams must not panic when a non-tagged node has an unhydrated User")
 }
 
diff --git a/hscontrol/policy/v2/tailscale_ssh_data_compat_test.go b/hscontrol/policy/v2/tailscale_ssh_data_compat_test.go
index 59342560f..79fc9b1a2 100644
--- a/hscontrol/policy/v2/tailscale_ssh_data_compat_test.go
+++ b/hscontrol/policy/v2/tailscale_ssh_data_compat_test.go
@@ -8,7 +8,10 @@
 package v2
 
 import (
+	"encoding/json"
+	"fmt"
 	"path/filepath"
+	"slices"
 	"strings"
 	"testing"
 
@@ -259,9 +262,89 @@ func TestSSHDataCompat(t *testing.T) {
 	}
 }
 
+// sshLocalUser maps sshUser to a local user the way tailssh does for one
+// rule: an exact entry wins, then "*"; "" means the rule does not apply.
+func sshLocalUser(users map[string]string, sshUser string) string {
+	local, ok := users[sshUser]
+	if !ok {
+		local = users["*"]
+	}
+
+	if local == "=" {
+		return sshUser
+	}
+
+	return local
+}
+
+// assertSSHCheckParamsMatchRules checks SSHCheckParams against check rules as
+// tailssh reads them: (src, dst, local user) must be found exactly when a
+// holdAndDelegate rule for dst lists src as a principal and maps some SSH
+// user to that local user.
+func assertSSHCheckParamsMatchRules(
+	t *testing.T,
+	pm *PolicyManager,
+	nodes types.Nodes,
+	rulesFor func(dst *types.Node) []*tailcfg.SSHRule,
+) {
+	t.Helper()
+
+	byIP := make(map[string]*types.Node)
+
+	for _, n := range nodes {
+		for _, ip := range n.IPs() {
+			byIP[ip.String()] = n
+		}
+	}
+
+	candidates := []string{"root", "nonroot-probe"}
+
+	for _, dst := range nodes {
+		for _, rule := range rulesFor(dst) {
+			for user := range rule.SSHUsers {
+				if user != "*" && !slices.Contains(candidates, user) {
+					candidates = append(candidates, user)
+				}
+			}
+		}
+	}
+
+	for _, dst := range nodes {
+		want := make(map[types.NodeID]map[string]bool)
+
+		for _, rule := range rulesFor(dst) {
+			if rule.Action == nil || rule.Action.HoldAndDelegate == "" {
+				continue
+			}
+
+			for _, p := range rule.Principals {
+				src, ok := byIP[p.NodeIP]
+				require.Truef(t, ok, "principal %q is not a node", p.NodeIP)
+
+				if want[src.ID] == nil {
+					want[src.ID] = make(map[string]bool)
+				}
+
+				for _, user := range candidates {
+					if local := sshLocalUser(rule.SSHUsers, user); local != "" {
+						want[src.ID][local] = true
+					}
+				}
+			}
+		}
+
+		for _, src := range nodes {
+			for _, user := range candidates {
+				_, got := pm.SSHCheckParams(src.ID, dst.ID, user)
+				assert.Equalf(t, want[src.ID][user], got,
+					"SSHCheckParams(%s -> %s as %s)", src.Hostname, dst.Hostname, user)
+			}
+		}
+	}
+}
+
 // TestSSHCheckParamsMatchesCaptures pins SSHCheckParams, which decides the
-// SSH check callback, to the check rules Tailscale sent: exactly the
-// captured holdAndDelegate principals must be found for each node.
+// SSH check callback, to the check rules Tailscale sent.
 func TestSSHCheckParamsMatchesCaptures(t *testing.T) {
 	t.Parallel()
 
@@ -291,36 +374,69 @@ func TestSSHCheckParamsMatchesCaptures(t *testing.T) {
 			)
 			require.NoError(t, err)
 
-			byIP := make(map[string]*types.Node)
-
-			for _, n := range nodes {
-				for _, ip := range n.IPs() {
-					byIP[ip.String()] = n
-				}
-			}
-
-			for _, dst := range nodes {
-				want := make(map[types.NodeID]bool)
-
-				for _, rule := range tf.Captures[dst.GivenName].SSHRules {
-					if rule.Action == nil || rule.Action.HoldAndDelegate == "" {
-						continue
-					}
-
-					for _, p := range rule.Principals {
-						src, ok := byIP[p.NodeIP]
-						require.Truef(t, ok, "principal %q is not a node", p.NodeIP)
-
-						want[src.ID] = true
-					}
-				}
-
-				for _, src := range nodes {
-					_, got := pm.SSHCheckParams(src.ID, dst.ID)
-					assert.Equalf(t, want[src.ID], got,
-						"SSHCheckParams(%s -> %s)", src.GivenName, dst.GivenName)
-				}
-			}
+			assertSSHCheckParamsMatchRules(t, pm, nodes,
+				func(dst *types.Node) []*tailcfg.SSHRule {
+					return tf.Captures[dst.GivenName].SSHRules
+				})
+		})
+	}
+}
+
+// TestSSHCheckParamsMatchesCompiledRules pins SSHCheckParams to headscale's
+// own compiled rules for shapes the captures lack, such as a user whose
+// email localpart is root.
+func TestSSHCheckParamsMatchesCompiledRules(t *testing.T) {
+	t.Parallel()
+
+	users := types.Users{
+		{Name: "root", Email: "root@example.com"},
+		{Name: "alice", Email: "alice@example.com"},
+	}
+	users[0].ID = 1
+	users[1].ID = 2
+
+	nodes := types.Nodes{
+		node("root-1", "100.64.0.1", "fd7a:115c:a1e0::1", users[0]),
+		node("root-2", "100.64.0.2", "fd7a:115c:a1e0::2", users[0]),
+		node("alice-1", "100.64.0.3", "fd7a:115c:a1e0::3", users[1]),
+		node("server", "100.64.0.4", "fd7a:115c:a1e0::4", users[1]),
+	}
+	for i, n := range nodes {
+		n.ID = types.NodeID(i + 1) //nolint:gosec
+	}
+
+	nodes[3].Tags = []string{"tag:server"}
+
+	check := func(dst string, users ...string) string {
+		usersJSON, err := json.Marshal(users)
+		require.NoError(t, err)
+
+		return fmt.Sprintf(`{"action": "check", "src": ["autogroup:member"], "dst": [%q], "users": %s}`,
+			dst, usersJSON)
+	}
+
+	for name, rules := range map[string][]string{
+		"localpart on tag":            {check("tag:server", "localpart:*@example.com")},
+		"localpart on self":           {check("autogroup:self", "localpart:*@example.com")},
+		"localpart then root":         {check("tag:server", "localpart:*@example.com"), check("autogroup:self", "root")},
+		"nonroot and literal on self": {check("autogroup:self", "autogroup:nonroot", "deploy")},
+	} {
+		t.Run(name, func(t *testing.T) {
+			t.Parallel()
+
+			pol := fmt.Sprintf(`{"tagOwners": {"tag:server": ["alice@"]}, "ssh": [%s]}`,
+				strings.Join(rules, ","))
+
+			pm, err := NewPolicyManager([]byte(pol), users, nodes.ViewSlice())
+			require.NoError(t, err)
+
+			assertSSHCheckParamsMatchRules(t, pm, nodes,
+				func(dst *types.Node) []*tailcfg.SSHRule {
+					sshPol, err := pm.SSHPolicy("", dst.View())
+					require.NoError(t, err)
+
+					return sshPol.Rules
+				})
 		})
 	}
 }
diff --git a/hscontrol/servertest/sshcheck_test.go b/hscontrol/servertest/sshcheck_test.go
index 73df0332a..020ded5e5 100644
--- a/hscontrol/servertest/sshcheck_test.go
+++ b/hscontrol/servertest/sshcheck_test.go
@@ -6,6 +6,7 @@ import (
 	"fmt"
 	"net/http"
 	"net/url"
+	"strconv"
 	"strings"
 	"testing"
 	"time"
@@ -15,6 +16,7 @@ import (
 	"github.com/stretchr/testify/assert"
 	"github.com/stretchr/testify/require"
 	"tailscale.com/tailcfg"
+	"tailscale.com/types/netmap"
 )
 
 // TestSSHCheckReDelegatesWhenSessionMissing exercises the fix for
@@ -45,7 +47,7 @@ func TestSSHCheckReDelegatesWhenSessionMissing(t *testing.T) {
 
 	// Sanity: the policy must actually subject this pair to a check, otherwise
 	// the test would pass for the wrong reason.
-	_, checkFound := h.Server.State().SSHCheckParams(srcID, dstID)
+	_, checkFound := h.Server.State().SSHCheckParams(srcID, dstID, sshCheckLocalUser)
 	require.True(t, checkFound, "test setup: (src, dst) must be subject to an SSH check")
 
 	// The dst node's first poll yields a real HoldAndDelegate carrying a real,
@@ -72,6 +74,9 @@ func TestSSHCheckReDelegatesWhenSessionMissing(t *testing.T) {
 		"re-delegation must mint a fresh auth_id")
 }
 
+// sshCheckLocalUser is the non-root local user the SSH-check polls log in as.
+const sshCheckLocalUser = "alice"
+
 // pollSSHAction issues an /machine/ssh/action poll from the given node over its
 // real Noise connection, as tailscaled does. An empty authID is the initial
 // poll; a non-empty one is a follow-up.
@@ -84,11 +89,20 @@ func pollSSHAction(
 ) tailcfg.SSHAction {
 	t.Helper()
 
-	actionURL := fmt.Sprintf("%s/machine/ssh/action/%d/to/%d", serverURL, srcID, dstID)
+	actionURL := fmt.Sprintf("%s/machine/ssh/action/%d/to/%d?local_user=%s",
+		serverURL, srcID, dstID, sshCheckLocalUser)
 	if authID != "" {
-		actionURL += "?auth_id=" + authID
+		actionURL += "&auth_id=" + authID
 	}
 
+	return pollSSHActionURL(t, node, actionURL)
+}
+
+// pollSSHActionURL polls actionURL from the given node over its real Noise
+// connection.
+func pollSSHActionURL(t *testing.T, node *servertest.TestClient, actionURL string) tailcfg.SSHAction {
+	t.Helper()
+
 	// Noise requests are addressed with the https scheme; the control client
 	// routes them over the established Noise connection (mirroring how
 	// controlclient issues its own register/map calls).
@@ -163,7 +177,7 @@ func TestSSHCheckRejectedAfterRuleRemoved(t *testing.T) {
 
 			h.ChangePolicy(t, []byte(after))
 
-			_, checkFound := h.Server.State().SSHCheckParams(srcID, dstID)
+			_, checkFound := h.Server.State().SSHCheckParams(srcID, dstID, sshCheckLocalUser)
 			require.False(t, checkFound, "test setup: check must be gone")
 
 			for poll, id := range map[string]string{"initial": "", "follow-up": authID.String()} {
@@ -174,3 +188,60 @@ func TestSSHCheckRejectedAfterRuleRemoved(t *testing.T) {
 		})
 	}
 }
+
+// expandHoldURL substitutes a HoldAndDelegate URL's variables literally, as
+// tailssh does before polling it.
+func expandHoldURL(holdURL string, srcID, dstID types.NodeID, localUser string) string {
+	return strings.NewReplacer(
+		"$SRC_NODE_ID", strconv.FormatUint(srcID.Uint64(), 10),
+		"$DST_NODE_ID", strconv.FormatUint(dstID.Uint64(), 10),
+		"$SSH_USER", url.QueryEscape(localUser),
+		"$LOCAL_USER", url.QueryEscape(localUser),
+	).Replace(holdURL)
+}
+
+// TestSSHCheckFollowsReturnedHoldURL walks a check the way tailssh does:
+// expand the HoldAndDelegate URL from the netmap, poll it, then poll the
+// URL the server returns. The follow-up must still carry the login user,
+// or a root-only rule denies a user who already authenticated.
+// https://github.com/juanfont/headscale/issues/3508
+func TestSSHCheckFollowsReturnedHoldURL(t *testing.T) {
+	t.Parallel()
+
+	h := servertest.NewHarness(t, 2)
+
+	srcID := types.NodeID(h.Client(0).Netmap().SelfNode.ID()) //nolint:gosec
+	dstID := types.NodeID(h.Client(1).Netmap().SelfNode.ID()) //nolint:gosec
+
+	h.ChangePolicy(t, []byte(`{"ssh": [{
+		"action": "check",
+		"src":    ["harness-default@"],
+		"dst":    ["autogroup:self"],
+		"users":  ["root"]
+	}]}`))
+
+	var ruleURL string
+
+	h.Client(1).WaitForCondition(t, "check rule in netmap", 10*time.Second,
+		func(nm *netmap.NetworkMap) bool {
+			if nm.SSHPolicy == nil || len(nm.SSHPolicy.Rules) == 0 ||
+				nm.SSHPolicy.Rules[0].Action == nil {
+				return false
+			}
+
+			ruleURL = nm.SSHPolicy.Rules[0].Action.HoldAndDelegate
+
+			return ruleURL != ""
+		})
+
+	initial := pollSSHActionURL(t, h.Client(1), expandHoldURL(ruleURL, srcID, dstID, "root"))
+	require.NotEmpty(t, initial.HoldAndDelegate, "check must hold, got %+v", initial)
+
+	auth, ok := h.Server.State().GetAuthCacheEntry(authIDFromHoldURL(t, initial.HoldAndDelegate))
+	require.True(t, ok)
+	auth.FinishAuth(types.AuthVerdict{})
+
+	followUp := pollSSHActionURL(t, h.Client(1),
+		expandHoldURL(initial.HoldAndDelegate, srcID, dstID, "root"))
+	assert.True(t, followUp.Accept, "authenticated root login must be accepted, got %+v", followUp)
+}
diff --git a/hscontrol/state/state.go b/hscontrol/state/state.go
index edc49174f..4b5747bd2 100644
--- a/hscontrol/state/state.go
+++ b/hscontrol/state/state.go
@@ -1260,12 +1260,13 @@ func (s *State) SSHPolicy(node types.NodeView) (*tailcfg.SSHPolicy, error) {
 	return s.polMan.SSHPolicy(s.cfg.ServerURL, node)
 }
 
-// SSHCheckParams resolves the SSH check period for a source-destination
-// node pair from the current policy.
+// SSHCheckParams resolves the SSH check period for src logging in to dst
+// as localUser from the current policy.
 func (s *State) SSHCheckParams(
 	srcNodeID, dstNodeID types.NodeID,
+	localUser string,
 ) (time.Duration, bool) {
-	return s.polMan.SSHCheckParams(srcNodeID, dstNodeID)
+	return s.polMan.SSHCheckParams(srcNodeID, dstNodeID, localUser)
 }
 
 // Filter returns the current network filter rules and matches.