diff --git a/e2e/agentnetwork/management_test.go b/e2e/agentnetwork/management_test.go
index cfd03f63c..6962f9796 100644
--- a/e2e/agentnetwork/management_test.go
+++ b/e2e/agentnetwork/management_test.go
@@ -160,8 +160,19 @@ func TestSettingsRoundTrip(t *testing.T) {
 	assert.Equal(t, before.Cluster, flipped.Cluster, "cluster must be immutable across updates")
 	assert.Equal(t, before.Subdomain, flipped.Subdomain, "subdomain must be immutable across updates")
 
+	// A cluster different from the pinned one must be rejected; echoing the
+	// pinned one back is valid.
+	_, err = srv.UpdateSettings(ctx, api.AgentNetworkSettingsRequest{
+		Cluster:                ptr("attacker.cluster.invalid"),
+		EnableLogCollection:    before.EnableLogCollection,
+		EnablePromptCollection: before.EnablePromptCollection,
+		RedactPii:              before.RedactPii,
+	})
+	requireClientError(t, err)
+
 	// Restore the original toggles.
 	_, err = srv.UpdateSettings(ctx, api.AgentNetworkSettingsRequest{
+		Cluster:                ptr(before.Cluster),
 		EnableLogCollection:    before.EnableLogCollection,
 		EnablePromptCollection: before.EnablePromptCollection,
 		RedactPii:              before.RedactPii,
diff --git a/management/internals/modules/agentnetwork/handlers/handlers_test.go b/management/internals/modules/agentnetwork/handlers/handlers_test.go
index 27ebea5dd..9d855c05d 100644
--- a/management/internals/modules/agentnetwork/handlers/handlers_test.go
+++ b/management/internals/modules/agentnetwork/handlers/handlers_test.go
@@ -17,6 +17,7 @@ import (
 
 	"github.com/netbirdio/netbird/management/internals/modules/agentnetwork"
 	agentNetworkTypes "github.com/netbirdio/netbird/management/internals/modules/agentnetwork/types"
+	"github.com/netbirdio/netbird/management/server/account"
 	nbcontext "github.com/netbirdio/netbird/management/server/context"
 	"github.com/netbirdio/netbird/management/server/permissions"
 	"github.com/netbirdio/netbird/management/server/store"
@@ -61,10 +62,23 @@ func newAgentNetworkHandlerFixture(t *testing.T) *agentNetworkHandlerFixture {
 		Return(true, context.Background(), nil).
 		AnyTimes()
 
-	manager := agentnetwork.NewManager(st, perms, nil, nil)
+	// Swallow activity events so the mutation paths (create/update/delete)
+	// are exercisable through the HTTP layer.
+	accounts := account.NewMockManager(ctrl)
+	accounts.EXPECT().
+		StoreEvent(gomock.Any(), gomock.Any(), gomock.Any(), gomock.Any(), gomock.Any(), gomock.Any()).
+		AnyTimes()
+	accounts.EXPECT().
+		UpdateAccountPeers(gomock.Any(), gomock.Any(), gomock.Any()).
+		AnyTimes()
+
+	manager := agentnetwork.NewManager(st, perms, accounts, nil)
 	h := &handler{manager: manager}
 
 	router := mux.NewRouter()
+	router.HandleFunc("/agent-network/providers", h.createProvider).Methods("POST")
+	router.HandleFunc("/agent-network/providers/{providerId}", h.getProvider).Methods("GET")
+	router.HandleFunc("/agent-network/providers/{providerId}", h.updateProvider).Methods("PUT")
 	h.addPolicyEndpoints(router)
 	h.addConsumptionEndpoints(router)
 	h.addBudgetRuleEndpoints(router)
diff --git a/management/internals/modules/agentnetwork/handlers/providers_handler.go b/management/internals/modules/agentnetwork/handlers/providers_handler.go
index c05363101..e0cd8b7c4 100644
--- a/management/internals/modules/agentnetwork/handlers/providers_handler.go
+++ b/management/internals/modules/agentnetwork/handlers/providers_handler.go
@@ -193,10 +193,19 @@ func (h *handler) updateProvider(w http.ResponseWriter, r *http.Request) {
 		return
 	}
 
-	provider := &types.Provider{
-		ID:        providerID,
-		AccountID: userAuth.AccountId,
+	// Overlay the request onto the stored row so omitted optional fields
+	// (models, extra_values, toggles, identity headers) keep their persisted
+	// values instead of silently resetting to zero — FromAPIRequest's
+	// nil-gating only works against the existing state.
+	existing, err := h.manager.GetProvider(r.Context(), userAuth.AccountId, userAuth.UserId, providerID)
+	if err != nil {
+		util.WriteError(r.Context(), err, w)
+		return
 	}
+	provider := existing.Copy()
+	// Blank the key so it is set only when the caller rotates it; the manager
+	// preserves the stored key for an empty value.
+	provider.APIKey = ""
 	provider.FromAPIRequest(&req)
 
 	updated, err := h.manager.UpdateProvider(r.Context(), userAuth.UserId, provider)
diff --git a/management/internals/modules/agentnetwork/handlers/providers_handler_test.go b/management/internals/modules/agentnetwork/handlers/providers_handler_test.go
index 649224c02..a1e90d298 100644
--- a/management/internals/modules/agentnetwork/handlers/providers_handler_test.go
+++ b/management/internals/modules/agentnetwork/handlers/providers_handler_test.go
@@ -1,7 +1,9 @@
 package handlers
 
 import (
+	"encoding/json"
 	"math"
+	nethttp "net/http"
 	"testing"
 
 	"github.com/stretchr/testify/assert"
@@ -51,3 +53,57 @@ func TestValidate_ModelRates(t *testing.T) {
 		assert.Error(t, validate(base(m), true), "case %q must be rejected", name)
 	}
 }
+
+// TestProviderHandler_UpdatePreservesOmittedFields is the anti-clobber guard
+// for PUT /agent-network/providers/{id}: the fields the OpenAPI schema
+// documents as omit-preserves — extra_values, metadata_disabled, identity
+// headers, enabled, skip_tls_verification, api_key — must keep their stored
+// values when absent from the request. Before the handler merged onto the
+// existing row, such an update silently wiped dashboard-configured
+// extra_values and reset the toggles account-wide. Models carry no such
+// contract: like the rest of the PUT payload they are replaced with what the
+// request says, so an omitted list clears.
+func TestProviderHandler_UpdatePreservesOmittedFields(t *testing.T) {
+	f := newAgentNetworkHandlerFixture(t)
+
+	create := `{
+        "provider_id": "openai_api",
+        "name": "openai",
+        "upstream_url": "https://api.openai.com",
+        "api_key": "sk-test",
+        "enabled": true,
+        "metadata_disabled": true,
+        "skip_tls_verification": true,
+        "extra_values": {"x-portkey-config": "pc-prod-3f2a"},
+        "identity_header_user_id": "x-bf-dim-netbird_user_id",
+        "models": [{"id": "gpt-4o", "input_per_1k": 0.0025, "output_per_1k": 0.01}]
+    }`
+	rec := f.do(t, nethttp.MethodPost, "/agent-network/providers", create)
+	require.Equal(t, nethttp.StatusOK, rec.Code, "create must succeed: %s", rec.Body.String())
+
+	var created api.AgentNetworkProvider
+	require.NoError(t, json.Unmarshal(rec.Body.Bytes(), &created))
+
+	// Minimal update: only the required fields (a rename), nothing optional.
+	update := `{"provider_id": "openai_api", "name": "openai-renamed", "upstream_url": "https://api.openai.com"}`
+	rec = f.do(t, nethttp.MethodPut, "/agent-network/providers/"+created.Id, update)
+	require.Equal(t, nethttp.StatusOK, rec.Code, "update must succeed: %s", rec.Body.String())
+
+	var updated api.AgentNetworkProvider
+	require.NoError(t, json.Unmarshal(rec.Body.Bytes(), &updated))
+	assert.Equal(t, "openai-renamed", updated.Name, "sent field must apply")
+	assert.True(t, updated.MetadataDisabled, "omitted metadata_disabled must be preserved")
+	assert.True(t, updated.SkipTlsVerification, "omitted skip_tls_verification must be preserved")
+	assert.True(t, updated.Enabled, "omitted enabled must be preserved")
+	require.NotNil(t, updated.ExtraValues, "omitted extra_values must be preserved")
+	assert.Equal(t, "pc-prod-3f2a", (*updated.ExtraValues)["x-portkey-config"], "stored extra value must survive the update")
+	assert.Equal(t, "x-bf-dim-netbird_user_id", updated.IdentityHeaderUserId, "omitted identity header must be preserved")
+	assert.Empty(t, updated.Models, "models carry no omit-preserves contract: an omitted list is replaced with empty")
+
+	// An explicit "" clears the identity header and stays on the wire.
+	clearHeader := `{"provider_id": "openai_api", "name": "openai-renamed", "upstream_url": "https://api.openai.com", "identity_header_user_id": ""}`
+	rec = f.do(t, nethttp.MethodPut, "/agent-network/providers/"+created.Id, clearHeader)
+	require.Equal(t, nethttp.StatusOK, rec.Code, "clearing update must succeed: %s", rec.Body.String())
+	assert.Contains(t, rec.Body.String(), `"identity_header_user_id":""`,
+		"cleared identity header must round-trip as an explicit empty string")
+}
diff --git a/management/internals/modules/agentnetwork/handlers/settings_handler.go b/management/internals/modules/agentnetwork/handlers/settings_handler.go
index c65efad0f..0d203867a 100644
--- a/management/internals/modules/agentnetwork/handlers/settings_handler.go
+++ b/management/internals/modules/agentnetwork/handlers/settings_handler.go
@@ -2,7 +2,6 @@ package handlers
 
 import (
 	"encoding/json"
-	"errors"
 	"net/http"
 
 	"github.com/gorilla/mux"
@@ -11,19 +10,20 @@ import (
 	nbcontext "github.com/netbirdio/netbird/management/server/context"
 	"github.com/netbirdio/netbird/shared/management/http/api"
 	"github.com/netbirdio/netbird/shared/management/http/util"
-	"github.com/netbirdio/netbird/shared/management/status"
 )
 
 // addSettingsEndpoints registers the Agent Network settings routes. The
-// settings row is bootstrapped server-side on first provider create; GET reads
-// it and PUT updates the mutable collection toggles (cluster/subdomain stay
-// immutable).
+// settings row is bootstrapped server-side on first provider create or on the
+// first PUT carrying a cluster; GET reads it and PUT applies a partial update
+// of the mutable collection toggles (cluster/subdomain stay immutable).
 func (h *handler) addSettingsEndpoints(router *mux.Router) {
 	router.HandleFunc("/agent-network/settings", h.getSettings).Methods("GET", "OPTIONS")
 	router.HandleFunc("/agent-network/settings", h.updateSettings).Methods("PUT", "OPTIONS")
 }
 
-// updateSettings applies the collection toggles to the account's settings row.
+// updateSettings replaces the mutable settings fields on the account's row.
+// A request carrying a cluster bootstraps the row when the account doesn't
+// have one yet.
 func (h *handler) updateSettings(w http.ResponseWriter, r *http.Request) {
 	userAuth, err := nbcontext.GetUserAuthFromContext(r.Context())
 	if err != nil {
@@ -48,11 +48,10 @@ func (h *handler) updateSettings(w http.ResponseWriter, r *http.Request) {
 	util.WriteJSONObject(r.Context(), w, updated.ToAPIResponse())
 }
 
-// getSettings returns the account's agent-network settings. The settings
-// row is bootstrapped on first provider create, so freshly-onboarded
-// accounts have nothing to read. Rather than 404-ing in that case (which
-// the dashboard would have to special-case), return a JSON null with 200
-// so consumers can branch on the body alone.
+// getSettings returns the account's agent-network settings. Freshly-onboarded
+// accounts have no settings row until a provider create (or a settings PUT
+// with a cluster) bootstraps one; per the OpenAPI contract that reads as a
+// plain 404.
 func (h *handler) getSettings(w http.ResponseWriter, r *http.Request) {
 	userAuth, err := nbcontext.GetUserAuthFromContext(r.Context())
 	if err != nil {
@@ -62,11 +61,6 @@ func (h *handler) getSettings(w http.ResponseWriter, r *http.Request) {
 
 	settings, err := h.manager.GetSettings(r.Context(), userAuth.AccountId, userAuth.UserId)
 	if err != nil {
-		var sErr *status.Error
-		if errors.As(err, &sErr) && sErr.Type() == status.NotFound {
-			util.WriteJSONObject(r.Context(), w, nil)
-			return
-		}
 		util.WriteError(r.Context(), err, w)
 		return
 	}
diff --git a/management/internals/modules/agentnetwork/handlers/settings_handler_test.go b/management/internals/modules/agentnetwork/handlers/settings_handler_test.go
new file mode 100644
index 000000000..a3a31856c
--- /dev/null
+++ b/management/internals/modules/agentnetwork/handlers/settings_handler_test.go
@@ -0,0 +1,122 @@
+package handlers
+
+import (
+	"encoding/json"
+	"net/http"
+	"testing"
+
+	"github.com/stretchr/testify/assert"
+	"github.com/stretchr/testify/require"
+
+	"github.com/netbirdio/netbird/shared/management/http/api"
+)
+
+// TestSettingsHandler_GetUnbootstrappedReturns404 pins the OpenAPI contract:
+// an account with no settings row answers a plain 404, never 200 with a
+// null/zero body, so API clients can rely on the status code alone.
+func TestSettingsHandler_GetUnbootstrappedReturns404(t *testing.T) {
+	f := newAgentNetworkHandlerFixture(t)
+
+	rec := f.do(t, http.MethodGet, "/agent-network/settings", "")
+	assert.Equal(t, http.StatusNotFound, rec.Code,
+		"unbootstrapped account must read as 404: got %d body=%s", rec.Code, rec.Body.String())
+	assert.NotEqual(t, "null", trimSpace(rec.Body.String()),
+		"the legacy 200+null shape must not come back")
+}
+
+// TestSettingsHandler_PutBootstrapsWithCluster covers the settings-first
+// bootstrap path: a PUT carrying a cluster on an unbootstrapped account
+// creates the row (cluster pinned, subdomain assigned) and applies the
+// mutable fields from the same request.
+func TestSettingsHandler_PutBootstrapsWithCluster(t *testing.T) {
+	f := newAgentNetworkHandlerFixture(t)
+
+	rec := f.do(t, http.MethodPut, "/agent-network/settings",
+		`{"cluster": "eu.proxy.netbird.io", "enable_log_collection": true, "enable_prompt_collection": true, "redact_pii": false, "access_log_retention_days": 30}`)
+	require.Equal(t, http.StatusOK, rec.Code, "bootstrap PUT must succeed: %s", rec.Body.String())
+
+	var got api.AgentNetworkSettings
+	require.NoError(t, json.Unmarshal(rec.Body.Bytes(), &got))
+	assert.Equal(t, "eu.proxy.netbird.io", got.Cluster, "cluster must be pinned from the request")
+	assert.NotEmpty(t, got.Subdomain, "subdomain must be assigned at bootstrap")
+	assert.Equal(t, got.Subdomain+".eu.proxy.netbird.io", got.Endpoint, "endpoint must combine subdomain and cluster")
+	assert.True(t, got.EnableLogCollection, "toggle from the bootstrap request must apply")
+	assert.True(t, got.EnablePromptCollection, "toggle from the bootstrap request must apply")
+	require.NotNil(t, got.AccessLogRetentionDays)
+	assert.Equal(t, 30, *got.AccessLogRetentionDays, "retention from the bootstrap request must apply")
+
+	// The row is now readable via GET.
+	rec = f.do(t, http.MethodGet, "/agent-network/settings", "")
+	require.Equal(t, http.StatusOK, rec.Code, "GET after bootstrap must succeed")
+}
+
+// TestSettingsHandler_PutWithoutClusterOnUnbootstrapped pins that a PUT
+// without a cluster cannot conjure a settings row out of nothing — there is
+// no cluster to pin — and surfaces as 404 like the GET.
+func TestSettingsHandler_PutWithoutClusterOnUnbootstrapped(t *testing.T) {
+	f := newAgentNetworkHandlerFixture(t)
+
+	rec := f.do(t, http.MethodPut, "/agent-network/settings",
+		`{"enable_log_collection": false, "enable_prompt_collection": false, "redact_pii": false}`)
+	assert.Equal(t, http.StatusNotFound, rec.Code,
+		"cluster-less PUT on an unbootstrapped account must 404: got %d body=%s", rec.Code, rec.Body.String())
+	assert.Contains(t, rec.Body.String(), "cluster",
+		"the error must point the caller at the bootstrap paths: %s", rec.Body.String())
+}
+
+// TestSettingsHandler_PutReplacesMutableFields pins the update contract shared
+// with the other PUT endpoints: the request replaces every mutable field, so a
+// toggle absent from the JSON lands as its zero value rather than being
+// preserved. Cluster and subdomain survive untouched.
+func TestSettingsHandler_PutReplacesMutableFields(t *testing.T) {
+	f := newAgentNetworkHandlerFixture(t)
+
+	rec := f.do(t, http.MethodPut, "/agent-network/settings",
+		`{"cluster": "eu.proxy.netbird.io", "enable_log_collection": true, "enable_prompt_collection": true, "redact_pii": true, "access_log_retention_days": 14}`)
+	require.Equal(t, http.StatusOK, rec.Code, "bootstrap PUT must succeed: %s", rec.Body.String())
+
+	var before api.AgentNetworkSettings
+	require.NoError(t, json.Unmarshal(rec.Body.Bytes(), &before))
+
+	rec = f.do(t, http.MethodPut, "/agent-network/settings",
+		`{"enable_log_collection": true, "enable_prompt_collection": false, "redact_pii": false}`)
+	require.Equal(t, http.StatusOK, rec.Code, "update PUT must succeed: %s", rec.Body.String())
+
+	var got api.AgentNetworkSettings
+	require.NoError(t, json.Unmarshal(rec.Body.Bytes(), &got))
+	assert.True(t, got.EnableLogCollection, "sent toggle must apply")
+	assert.False(t, got.EnablePromptCollection, "sent toggle must apply")
+	assert.False(t, got.RedactPii, "sent toggle must apply")
+	require.NotNil(t, got.AccessLogRetentionDays)
+	assert.Equal(t, 0, *got.AccessLogRetentionDays,
+		"retention absent from the request must land as the zero value — PUT replaces all mutable fields")
+	assert.Equal(t, before.Cluster, got.Cluster, "cluster must survive updates untouched")
+	assert.Equal(t, before.Subdomain, got.Subdomain, "subdomain must survive updates untouched")
+}
+
+// TestSettingsHandler_PutRejectsClusterChange pins cluster immutability: once
+// assigned, a differing cluster is rejected as a validation error instead of
+// being silently ignored, so callers never observe a value other than the one
+// they sent. Echoing the assigned cluster back stays valid, which lets
+// declarative clients send their full desired state idempotently.
+func TestSettingsHandler_PutRejectsClusterChange(t *testing.T) {
+	f := newAgentNetworkHandlerFixture(t)
+
+	rec := f.do(t, http.MethodPut, "/agent-network/settings",
+		`{"cluster": "eu.proxy.netbird.io", "enable_log_collection": true, "enable_prompt_collection": false, "redact_pii": false}`)
+	require.Equal(t, http.StatusOK, rec.Code, "bootstrap PUT must succeed: %s", rec.Body.String())
+
+	rec = f.do(t, http.MethodPut, "/agent-network/settings",
+		`{"cluster": "us.proxy.netbird.io", "enable_log_collection": true, "enable_prompt_collection": false, "redact_pii": false}`)
+	assert.Equal(t, http.StatusUnprocessableEntity, rec.Code,
+		"cluster change must be rejected as a validation error: got %d body=%s", rec.Code, rec.Body.String())
+
+	rec = f.do(t, http.MethodPut, "/agent-network/settings",
+		`{"cluster": "eu.proxy.netbird.io", "enable_log_collection": true, "enable_prompt_collection": false, "redact_pii": true}`)
+	require.Equal(t, http.StatusOK, rec.Code, "echoing the assigned cluster must stay valid: %s", rec.Body.String())
+
+	var got api.AgentNetworkSettings
+	require.NoError(t, json.Unmarshal(rec.Body.Bytes(), &got))
+	assert.Equal(t, "eu.proxy.netbird.io", got.Cluster, "cluster must be unchanged")
+	assert.True(t, got.RedactPii, "toggle sent alongside the echoed cluster must apply")
+}
diff --git a/management/internals/modules/agentnetwork/manager.go b/management/internals/modules/agentnetwork/manager.go
index 77c77ce44..4ecb8786f 100644
--- a/management/internals/modules/agentnetwork/manager.go
+++ b/management/internals/modules/agentnetwork/manager.go
@@ -554,19 +554,38 @@ func (m *managerImpl) DeleteBudgetRule(ctx context.Context, accountID, userID, r
 	return nil
 }
 
-// UpdateSettings applies the mutable account-level settings — the collection
-// toggles — onto the existing row. Cluster and Subdomain are immutable and are
-// preserved from the persisted row regardless of the input. Because the
-// collection toggles change the synthesised service config (prompt-capture
-// gating, access-log emission), a reconcile is triggered so the proxy and peer
-// network maps converge on the new state.
+// UpdateSettings replaces the mutable account-level settings — the collection
+// toggles and retention — on the account's row. When the account has no
+// settings row yet, a non-empty settings.Cluster bootstraps one (same path as
+// first provider create); without it the update fails with NotFound. On an
+// existing row the cluster and subdomain are immutable: a differing
+// settings.Cluster is rejected rather than silently ignored so callers never
+// observe a value other than what they sent. Because the collection toggles
+// change the synthesised service config (prompt-capture gating, access-log
+// emission), a reconcile is triggered so the proxy and peer network maps
+// converge on the new state.
 func (m *managerImpl) UpdateSettings(ctx context.Context, userID string, settings *types.Settings) (*types.Settings, error) {
 	if err := m.requirePermission(ctx, settings.AccountID, userID, operations.Update); err != nil {
 		return nil, err
 	}
 
+	requestedCluster := strings.TrimSpace(settings.Cluster)
+
 	existing, err := m.store.GetAgentNetworkSettings(ctx, store.LockingStrengthUpdate, settings.AccountID)
-	if err != nil {
+	switch {
+	case err == nil:
+		if requestedCluster != "" && requestedCluster != existing.Cluster {
+			return nil, status.Errorf(status.InvalidArgument, "cluster is immutable once assigned (current: %s)", existing.Cluster)
+		}
+	case isNotFound(err):
+		if requestedCluster == "" {
+			return nil, status.Errorf(status.NotFound, "agent network settings have not been bootstrapped yet; pass cluster to bootstrap them, or create a provider with bootstrap_cluster set")
+		}
+		existing, err = m.bootstrapSettingsIfNeeded(ctx, settings.AccountID, requestedCluster)
+		if err != nil {
+			return nil, err
+		}
+	default:
 		return nil, fmt.Errorf("get agent network settings: %w", err)
 	}
 
@@ -590,6 +609,12 @@ func (m *managerImpl) UpdateSettings(ctx context.Context, userID string, setting
 	return existing, nil
 }
 
+// isNotFound reports whether err is a status.NotFound error.
+func isNotFound(err error) bool {
+	var sErr *status.Error
+	return errors.As(err, &sErr) && sErr.Type() == status.NotFound
+}
+
 // validateProviderRefs ensures every destination provider id refers to a
 // provider that exists in the same account.
 func (m *managerImpl) validateProviderRefs(ctx context.Context, accountID string, providerIDs []string) error {
diff --git a/management/internals/modules/agentnetwork/types/provider.go b/management/internals/modules/agentnetwork/types/provider.go
index 96242f45f..cc0bece7a 100644
--- a/management/internals/modules/agentnetwork/types/provider.go
+++ b/management/internals/modules/agentnetwork/types/provider.go
@@ -192,16 +192,20 @@ func (p *Provider) ToAPIResponse() *api.AgentNetworkProvider {
 	created := p.CreatedAt
 	updated := p.UpdatedAt
 	resp := &api.AgentNetworkProvider{
-		Id:                  p.ID,
-		ProviderId:          p.ProviderID,
-		Name:                p.Name,
-		UpstreamUrl:         p.UpstreamURL,
-		Models:              models,
-		Enabled:             p.Enabled,
-		SkipTlsVerification: p.SkipTLSVerification,
-		MetadataDisabled:    p.MetadataDisabled,
-		CreatedAt:           &created,
-		UpdatedAt:           &updated,
+		Id:          p.ID,
+		ProviderId:  p.ProviderID,
+		Name:        p.Name,
+		UpstreamUrl: p.UpstreamURL,
+		Models:      models,
+		// Always present on the wire so an explicitly cleared header
+		// round-trips as "" instead of vanishing from the response.
+		IdentityHeaderUserId: p.IdentityHeaderUserID,
+		IdentityHeaderGroups: p.IdentityHeaderGroups,
+		Enabled:              p.Enabled,
+		SkipTlsVerification:  p.SkipTLSVerification,
+		MetadataDisabled:     p.MetadataDisabled,
+		CreatedAt:            &created,
+		UpdatedAt:            &updated,
 	}
 	if len(p.ExtraValues) > 0 {
 		out := make(map[string]string, len(p.ExtraValues))
@@ -210,14 +214,6 @@ func (p *Provider) ToAPIResponse() *api.AgentNetworkProvider {
 		}
 		resp.ExtraValues = &out
 	}
-	if p.IdentityHeaderUserID != "" {
-		v := p.IdentityHeaderUserID
-		resp.IdentityHeaderUserId = &v
-	}
-	if p.IdentityHeaderGroups != "" {
-		v := p.IdentityHeaderGroups
-		resp.IdentityHeaderGroups = &v
-	}
 	return resp
 }
 
diff --git a/management/internals/modules/agentnetwork/types/provider_test.go b/management/internals/modules/agentnetwork/types/provider_test.go
index f9756bb8b..fd553ece2 100644
--- a/management/internals/modules/agentnetwork/types/provider_test.go
+++ b/management/internals/modules/agentnetwork/types/provider_test.go
@@ -77,3 +77,41 @@ func TestProvider_MetadataDisabled_RoundTrip(t *testing.T) {
 	assert.False(t, p.MetadataDisabled, "explicit false must clear metadata_disabled")
 	assert.False(t, p.ToAPIResponse().MetadataDisabled, "response must reflect the cleared value")
 }
+
+// TestProvider_IdentityHeaders_AlwaysOnWire pins that the identity header
+// fields are always present in the API response — an explicitly cleared
+// ("") header must round-trip as "" rather than vanish, so API consumers
+// (e.g. the Terraform provider) never observe a value other than the one
+// they wrote.
+func TestProvider_IdentityHeaders_AlwaysOnWire(t *testing.T) {
+	set := "x-bf-dim-netbird_user_id"
+	empty := ""
+
+	base := func() *api.AgentNetworkProviderRequest {
+		return &api.AgentNetworkProviderRequest{
+			ProviderId:  "custom",
+			Name:        "bifrost",
+			UpstreamUrl: "https://bifrost.internal",
+		}
+	}
+
+	p := NewProvider("acc-1")
+	resp := p.ToAPIResponse()
+	assert.Equal(t, "", resp.IdentityHeaderUserId, "unset header must surface as empty string, not be omitted")
+	assert.Equal(t, "", resp.IdentityHeaderGroups, "unset header must surface as empty string, not be omitted")
+
+	req := base()
+	req.IdentityHeaderUserId = &set
+	p.FromAPIRequest(req)
+	assert.Equal(t, set, p.ToAPIResponse().IdentityHeaderUserId, "configured header must round-trip")
+
+	// Omitting the field preserves it.
+	p.FromAPIRequest(base())
+	assert.Equal(t, set, p.ToAPIResponse().IdentityHeaderUserId, "omitted header must preserve the stored value")
+
+	// An explicit "" clears it AND stays visible on the wire.
+	req = base()
+	req.IdentityHeaderUserId = &empty
+	p.FromAPIRequest(req)
+	assert.Equal(t, "", p.ToAPIResponse().IdentityHeaderUserId, "cleared header must round-trip as empty string")
+}
diff --git a/management/internals/modules/agentnetwork/types/settings.go b/management/internals/modules/agentnetwork/types/settings.go
index d61d9deff..3c2328e65 100644
--- a/management/internals/modules/agentnetwork/types/settings.go
+++ b/management/internals/modules/agentnetwork/types/settings.go
@@ -1,6 +1,7 @@
 package types
 
 import (
+	"strings"
 	"time"
 
 	"github.com/netbirdio/netbird/shared/management/http/api"
@@ -66,9 +67,15 @@ func (s *Settings) ToAPIResponse() *api.AgentNetworkSettings {
 	}
 }
 
-// FromAPIRequest applies the mutable settings fields from the request. Cluster
-// and Subdomain are immutable and intentionally not touched here.
+// FromAPIRequest applies the request onto the receiver. The mutable
+// collection fields are always replaced with the request values. Cluster
+// participates only in bootstrap and the immutability check (see
+// Manager.UpdateSettings); Subdomain is server-assigned and never taken
+// from a request.
 func (s *Settings) FromAPIRequest(req *api.AgentNetworkSettingsRequest) {
+	if req.Cluster != nil {
+		s.Cluster = strings.TrimSpace(*req.Cluster)
+	}
 	s.EnableLogCollection = req.EnableLogCollection
 	s.EnablePromptCollection = req.EnablePromptCollection
 	s.RedactPii = req.RedactPii
diff --git a/management/server/agentnetwork_budgetrule_realstack_test.go b/management/server/agentnetwork_budgetrule_realstack_test.go
index d17f2e26a..790285b4e 100644
--- a/management/server/agentnetwork_budgetrule_realstack_test.go
+++ b/management/server/agentnetwork_budgetrule_realstack_test.go
@@ -102,11 +102,20 @@ func TestAgentNetwork_UpdateSettings_PreservesImmutableAndTogglesCollection(t *t
 	require.NotEmpty(t, before.Subdomain, "subdomain pinned at bootstrap")
 	assert.False(t, before.EnablePromptCollection, "prompt collection defaults off")
 
-	// Attempt to flip toggles AND smuggle a different cluster/subdomain — the
-	// immutable fields must be ignored.
+	// A cluster different from the one pinned at bootstrap must be rejected
+	// outright — never silently swapped or ignored.
+	_, err = mgr.UpdateSettings(ctx, adminUserID, &agenttypes.Settings{
+		AccountID:           accountID,
+		Cluster:             "attacker.cluster",
+		EnableLogCollection: true,
+	})
+	require.Error(t, err, "UpdateSettings with a mismatched cluster must fail")
+
+	// Flipping the toggles works with the pinned cluster echoed back (and
+	// with it omitted); the subdomain is never taken from the request.
 	updated, err := mgr.UpdateSettings(ctx, adminUserID, &agenttypes.Settings{
 		AccountID:              accountID,
-		Cluster:                "attacker.cluster",
+		Cluster:                clusterAddr,
 		Subdomain:              "evil",
 		EnableLogCollection:    true,
 		EnablePromptCollection: true,
diff --git a/shared/management/http/api/openapi.yml b/shared/management/http/api/openapi.yml
index 8ad3d932c..2473c8319 100644
--- a/shared/management/http/api/openapi.yml
+++ b/shared/management/http/api/openapi.yml
@@ -5149,12 +5149,12 @@ components:
         identity_header_user_id:
           type: string
           description: |
-            Wire header name the proxy stamps with the caller's display identity (user email or peer name) when the catalog entry's HeaderPair is `customizable`. Empty disables stamping for this dimension. Ignored when the catalog entry has a fixed HeaderPair (e.g. LiteLLM, Portkey). Used today by Bifrost: typical values are `x-bf-lh-netbird_user_id` (always-on log metadata) or `x-bf-dim-netbird_user_id` (Prometheus / OTEL — requires the label to be pre-declared in the gateway's `client.prometheus_labels` config).
+            Wire header name the proxy stamps with the caller's display identity (user email or peer name) when the catalog entry's HeaderPair is `customizable`. Always present in responses; empty disables stamping for this dimension. Ignored when the catalog entry has a fixed HeaderPair (e.g. LiteLLM, Portkey). Used today by Bifrost: typical values are `x-bf-lh-netbird_user_id` (always-on log metadata) or `x-bf-dim-netbird_user_id` (Prometheus / OTEL — requires the label to be pre-declared in the gateway's `client.prometheus_labels` config).
           example: "x-bf-dim-netbird_user_id"
         identity_header_groups:
           type: string
           description: |
-            Wire header name the proxy stamps with the caller's NetBird groups as a comma-separated list (sorted) when the catalog entry's HeaderPair is `customizable`. Empty disables stamping for this dimension. Same per-catalog semantics as `identity_header_user_id`.
+            Wire header name the proxy stamps with the caller's NetBird groups as a comma-separated list (sorted) when the catalog entry's HeaderPair is `customizable`. Always present in responses; empty disables stamping for this dimension. Same per-catalog semantics as `identity_header_user_id`.
           example: "x-bf-dim-netbird_groups"
         enabled:
           type: boolean
@@ -5186,6 +5186,8 @@ components:
         - name
         - upstream_url
         - models
+        - identity_header_user_id
+        - identity_header_groups
         - enabled
         - skip_tls_verification
         - metadata_disabled
@@ -5222,7 +5224,7 @@ components:
         extra_values:
           type: object
           description: |
-            Operator-typed values for catalog-declared extra headers (see AgentNetworkProvider.extra_values). When present on a request, the whole map replaces the stored values. Empty strings drop the corresponding key.
+            Operator-typed values for catalog-declared extra headers (see AgentNetworkProvider.extra_values). When present on a request, the whole map replaces the stored values; when omitted the stored values are left unchanged. Empty strings drop the corresponding key.
           additionalProperties:
             type: string
           example:
@@ -6244,8 +6246,12 @@ components:
         - updated_at
     AgentNetworkSettingsRequest:
       type: object
-      description: Mutable account-level Agent Network settings. Cluster and subdomain are immutable and not accepted here.
+      description: Account-level Agent Network settings update. The request replaces every mutable field. `cluster` additionally bootstraps the per-account settings row when the account does not have one yet; the subdomain is always server-assigned.
       properties:
+        cluster:
+          type: string
+          description: Address of the NetBird proxy cluster fronting this account's agent-network endpoint. When the account has no settings row yet, providing it bootstraps the row (assigning the subdomain that forms the agent endpoint). The cluster is immutable once assigned — later updates must omit it or send the assigned value; any other value is rejected.
+          example: "eu.proxy.netbird.io"
         enable_log_collection:
           type: boolean
           description: Whether per-request access-log entries are collected for this account's agent-network traffic.
@@ -13690,7 +13696,7 @@ paths:
   /api/agent-network/settings:
     get:
       summary: Retrieve Agent Network settings
-      description: Returns the per-account Agent Network gateway settings (cluster, subdomain, endpoint). Returns 404 when no provider has been created yet — settings are lazily bootstrapped on first provider create.
+      description: Returns the per-account Agent Network gateway settings (cluster, subdomain, endpoint). Returns 404 when the account has not been bootstrapped yet — settings are bootstrapped on first provider create (`bootstrap_cluster`) or via PUT with `cluster`.
       tags: [ Agent Network ]
       security:
         - BearerAuth: [ ]
@@ -13712,7 +13718,7 @@ paths:
           "$ref": "#/components/responses/internal_error"
     put:
       summary: Update Agent Network settings
-      description: Updates the mutable account-level Agent Network settings (collection toggles). Cluster and subdomain are immutable and ignored if sent. Returns 404 when settings have not been bootstrapped (no provider created yet).
+      description: Updates the account-level Agent Network settings; the request replaces every mutable field (collection toggles and retention). When the account has no settings row yet, providing `cluster` bootstraps it (assigning the subdomain that forms the agent endpoint); without `cluster` the request returns 404. Sending a `cluster` different from the assigned one is rejected (the cluster is immutable once assigned). The subdomain is always server-assigned and immutable.
       tags: [ Agent Network ]
       security:
         - BearerAuth: [ ]
@@ -13738,6 +13744,8 @@ paths:
           "$ref": "#/components/responses/forbidden"
         '404':
           "$ref": "#/components/responses/not_found"
+        '422':
+          "$ref": "#/components/responses/validation_failed"
         '500':
           "$ref": "#/components/responses/internal_error"
   /api/agent-network/budget-rules:
diff --git a/shared/management/http/api/types.gen.go b/shared/management/http/api/types.gen.go
index 87dd9ccfc..b20c046e9 100644
--- a/shared/management/http/api/types.gen.go
+++ b/shared/management/http/api/types.gen.go
@@ -2275,11 +2275,11 @@ type AgentNetworkProvider struct {
 	// Id Provider ID
 	Id string `json:"id"`
 
-	// IdentityHeaderGroups Wire header name the proxy stamps with the caller's NetBird groups as a comma-separated list (sorted) when the catalog entry's HeaderPair is `customizable`. Empty disables stamping for this dimension. Same per-catalog semantics as `identity_header_user_id`.
-	IdentityHeaderGroups *string `json:"identity_header_groups,omitempty"`
+	// IdentityHeaderGroups Wire header name the proxy stamps with the caller's NetBird groups as a comma-separated list (sorted) when the catalog entry's HeaderPair is `customizable`. Always present in responses; empty disables stamping for this dimension. Same per-catalog semantics as `identity_header_user_id`.
+	IdentityHeaderGroups string `json:"identity_header_groups"`
 
-	// IdentityHeaderUserId Wire header name the proxy stamps with the caller's display identity (user email or peer name) when the catalog entry's HeaderPair is `customizable`. Empty disables stamping for this dimension. Ignored when the catalog entry has a fixed HeaderPair (e.g. LiteLLM, Portkey). Used today by Bifrost: typical values are `x-bf-lh-netbird_user_id` (always-on log metadata) or `x-bf-dim-netbird_user_id` (Prometheus / OTEL — requires the label to be pre-declared in the gateway's `client.prometheus_labels` config).
-	IdentityHeaderUserId *string `json:"identity_header_user_id,omitempty"`
+	// IdentityHeaderUserId Wire header name the proxy stamps with the caller's display identity (user email or peer name) when the catalog entry's HeaderPair is `customizable`. Always present in responses; empty disables stamping for this dimension. Ignored when the catalog entry has a fixed HeaderPair (e.g. LiteLLM, Portkey). Used today by Bifrost: typical values are `x-bf-lh-netbird_user_id` (always-on log metadata) or `x-bf-dim-netbird_user_id` (Prometheus / OTEL — requires the label to be pre-declared in the gateway's `client.prometheus_labels` config).
+	IdentityHeaderUserId string `json:"identity_header_user_id"`
 
 	// MetadataDisabled Whether identity metadata injection is disabled for this provider. When enabled (the default), the proxy stamps the caller's user and authorizing group onto upstream requests as provider-specific metadata (e.g. AWS Bedrock's X-Amzn-Bedrock-Request-Metadata header). Set true to suppress it.
 	MetadataDisabled bool `json:"metadata_disabled"`
@@ -2335,7 +2335,7 @@ type AgentNetworkProviderRequest struct {
 	// Enabled Whether the provider is enabled. Defaults to true on create.
 	Enabled *bool `json:"enabled,omitempty"`
 
-	// ExtraValues Operator-typed values for catalog-declared extra headers (see AgentNetworkProvider.extra_values). When present on a request, the whole map replaces the stored values. Empty strings drop the corresponding key.
+	// ExtraValues Operator-typed values for catalog-declared extra headers (see AgentNetworkProvider.extra_values). When present on a request, the whole map replaces the stored values; when omitted the stored values are left unchanged. Empty strings drop the corresponding key.
 	ExtraValues *map[string]string `json:"extra_values,omitempty"`
 
 	// IdentityHeaderGroups Wire header name for the caller's groups CSV. See AgentNetworkProvider.identity_header_groups. Same omit / empty semantics as `identity_header_user_id`.
@@ -2393,11 +2393,14 @@ type AgentNetworkSettings struct {
 	UpdatedAt *time.Time `json:"updated_at,omitempty"`
 }
 
-// AgentNetworkSettingsRequest Mutable account-level Agent Network settings. Cluster and subdomain are immutable and not accepted here.
+// AgentNetworkSettingsRequest Account-level Agent Network settings update. The request replaces every mutable field. `cluster` additionally bootstraps the per-account settings row when the account does not have one yet; the subdomain is always server-assigned.
 type AgentNetworkSettingsRequest struct {
 	// AccessLogRetentionDays Days to retain full access-log rows; older rows are swept. 0 or less means keep indefinitely.
 	AccessLogRetentionDays *int `json:"access_log_retention_days,omitempty"`
 
+	// Cluster Address of the NetBird proxy cluster fronting this account's agent-network endpoint. When the account has no settings row yet, providing it bootstraps the row (assigning the subdomain that forms the agent endpoint). The cluster is immutable once assigned — later updates must omit it or send the assigned value; any other value is rejected.
+	Cluster *string `json:"cluster,omitempty"`
+
 	// EnableLogCollection Whether per-request access-log entries are collected for this account's agent-network traffic.
 	EnableLogCollection bool `json:"enable_log_collection"`