diff --git a/cfapi/base_client.go b/cfapi/base_client.go
index 05e32a83edb..7663fc98a68 100644
--- a/cfapi/base_client.go
+++ b/cfapi/base_client.go
@@ -40,6 +40,7 @@ type baseEndpoints struct {
 	zoneLevel     url.URL
 	accountRoutes url.URL
 	accountVnets  url.URL
+	zones         url.URL
 }
 
 var _ Client = (*RESTClient)(nil)
@@ -60,7 +61,11 @@ func NewRESTClient(baseURL, accountTag, zoneTag, authToken, userAgent string, lo
 	}
 	zoneLevelEndpoint, err := url.Parse(fmt.Sprintf("%s/zones/%s/tunnels", baseURL, zoneTag))
 	if err != nil {
-		return nil, errors.Wrap(err, "failed to create account level endpoint")
+		return nil, errors.Wrap(err, "failed to create zone level endpoint")
+	}
+	zonesEndpoint, err := url.Parse(fmt.Sprintf("%s/zones", baseURL))
+	if err != nil {
+		return nil, errors.Wrap(err, "failed to create zones endpoint")
 	}
 	httpTransport := http.Transport{
 		TLSHandshakeTimeout:   defaultTimeout,
@@ -73,6 +78,7 @@ func NewRESTClient(baseURL, accountTag, zoneTag, authToken, userAgent string, lo
 			zoneLevel:     *zoneLevelEndpoint,
 			accountRoutes: *accountRoutesEndpoint,
 			accountVnets:  *accountVnetsEndpoint,
+			zones:         *zonesEndpoint,
 		},
 		authToken: authToken,
 		userAgent: userAgent,
@@ -241,3 +247,16 @@ func (r *RESTClient) statusCodeToError(op string, resp *http.Response) error {
 	return errors.Errorf("API call to %s failed with status %d: %s", op,
 		resp.StatusCode, http.StatusText(resp.StatusCode))
 }
+
+func (r *RESTClient) ListZones() ([]*Zone, error) {
+	endpoint := r.baseEndpoints.zones
+	return fetchExhaustively[Zone](func(page int) (*http.Response, error) {
+		reqURL := endpoint
+		query := reqURL.Query()
+		query.Set("page", fmt.Sprintf("%d", page))
+		query.Set("per_page", "50")
+		// Required to get basic zone info instead of just IDs
+		reqURL.RawQuery = query.Encode()
+		return r.sendRequest("GET", reqURL, nil)
+	})
+}
diff --git a/cfapi/client.go b/cfapi/client.go
index 1d08cc50cdb..55c914f5ba9 100644
--- a/cfapi/client.go
+++ b/cfapi/client.go
@@ -17,6 +17,7 @@ type TunnelClient interface {
 
 type HostnameClient interface {
 	RouteTunnel(tunnelID uuid.UUID, route HostnameRoute) (HostnameRouteResult, error)
+	ListZones() ([]*Zone, error)
 }
 
 type IPRouteClient interface {
@@ -39,3 +40,8 @@ type Client interface {
 	IPRouteClient
 	VnetClient
 }
+
+type Zone struct {
+	ID   string `json:"id"`
+	Name string `json:"name"`
+}
diff --git a/cfapi/hostname.go b/cfapi/hostname.go
index b8ca8bd441c..115bf613b59 100644
--- a/cfapi/hostname.go
+++ b/cfapi/hostname.go
@@ -5,7 +5,9 @@ import (
 	"fmt"
 	"io"
 	"net/http"
+	"net/url"
 	"path"
+	"strings"
 
 	"github.com/google/uuid"
 	"github.com/pkg/errors"
@@ -25,6 +27,7 @@ type HostnameRoute interface {
 	RecordType() string
 	UnmarshalResult(body io.Reader) (HostnameRouteResult, error)
 	String() string
+	Hostname() string
 }
 
 type HostnameRouteResult interface {
@@ -78,6 +81,10 @@ func (dr *DNSRoute) String() string {
 	return fmt.Sprintf("%s %s", dr.RecordType(), dr.userHostname)
 }
 
+func (dr *DNSRoute) Hostname() string {
+	return dr.userHostname
+}
+
 func (res *DNSRouteResult) SuccessSummary() string {
 	var msgFmt string
 	switch res.CName {
@@ -139,6 +146,10 @@ func (lb *LBRoute) String() string {
 	return fmt.Sprintf("%s %s %s", lb.RecordType(), lb.lbName, lb.lbPool)
 }
 
+func (lr *LBRoute) Hostname() string {
+	return lr.lbName
+}
+
 func (lr *LBRoute) UnmarshalResult(body io.Reader) (HostnameRouteResult, error) {
 	var result LBRouteResult
 	err := parseResponse(body, &result)
@@ -176,7 +187,35 @@ func (res *LBRouteResult) SuccessSummary() string {
 }
 
 func (r *RESTClient) RouteTunnel(tunnelID uuid.UUID, route HostnameRoute) (HostnameRouteResult, error) {
+	// First, try to find the correct zone by fetching all zones and matching the hostname
+	zoneID := ""
+	zones, err := r.ListZones()
+	if err == nil {
+		longestMatch := ""
+		for _, zone := range zones {
+			// A hostname should end with the zone name EXACTLY or be a subdomain of it.
+			// e.g. "app.staging.example.com" ends with ".example.com" and "example.com" == "example.com"
+			if route.Hostname() == zone.Name || strings.HasSuffix(route.Hostname(), "."+zone.Name) {
+				// We want the most specific zone if there are multiple matches
+				// e.g. "staging.example.com" zone vs "example.com" zone
+				if len(zone.Name) > len(longestMatch) {
+					longestMatch = zone.Name
+					zoneID = zone.ID
+				}
+			}
+		}
+	}
+
 	endpoint := r.baseEndpoints.zoneLevel
+	if zoneID != "" {
+		// Construct dynamic endpoint using the correct zone ID instead of the default one
+		baseURL := strings.TrimSuffix(r.baseEndpoints.zones.String(), "/zones")
+		zoneEndpoint, err := url.Parse(fmt.Sprintf("%s/zones/%s/tunnels", baseURL, zoneID))
+		if err == nil {
+			endpoint = *zoneEndpoint
+		}
+	}
+
 	endpoint.Path = path.Join(endpoint.Path, fmt.Sprintf("%v/routes", tunnelID))
 	resp, err := r.sendRequest("PUT", endpoint, route)
 	if err != nil {
diff --git a/cfapi/hostname_test.go b/cfapi/hostname_test.go
index 5100465a39b..86e4265f6c5 100644
--- a/cfapi/hostname_test.go
+++ b/cfapi/hostname_test.go
@@ -1,9 +1,14 @@
 package cfapi
 
 import (
+	"io"
+	"net/http"
+	"net/http/httptest"
 	"strings"
 	"testing"
 
+	"github.com/google/uuid"
+	"github.com/rs/zerolog"
 	"github.com/stretchr/testify/assert"
 )
 
@@ -97,3 +102,73 @@ func TestLBRouteResultSuccessSummary(t *testing.T) {
 		assert.Equal(t, tt.expected, actual, "case %d", i+1)
 	}
 }
+
+func TestRouteTunnel_ZoneResolution(t *testing.T) {
+	ts := httptest.NewServer(http.HandlerFunc(func(w http.ResponseWriter, r *http.Request) {
+		if r.URL.Path == "/zones" {
+			// A sample JSON response matching the Cloudflare api format, ensuring we mimic what the real API sends.
+			io.WriteString(w, `{
+				"success": true,
+				"errors": [],
+				"messages": [],
+				"result": [
+					{
+						"id": "zone-1",
+						"name": "example.com",
+						"status": "active",
+						"paused": false
+					},
+					{
+						"id": "zone-2",
+						"name": "example.co.uk",
+						"status": "active",
+						"paused": false
+					}
+				],
+				"result_info": {
+					"page": 1,
+					"per_page": 50,
+					"total_pages": 1,
+					"count": 2,
+					"total_count": 2
+				}
+			}`)
+			return
+		}
+		if r.URL.Path == "/zones/zone-1/tunnels/11111111-2222-3333-4444-555555555555/routes" {
+			io.WriteString(w, `{"success":true,"result":{"cname":"new","name":"app.example.com"}}`)
+			return
+		}
+		
+		// Fallback path when zone does NOT match. It uses "default-zone-from-login" as specified in NewRESTClient arguments.
+		if r.URL.Path == "/zones/default-zone-from-login/tunnels/11111111-2222-3333-4444-555555555555/routes" {
+			io.WriteString(w, `{"success":true,"result":{"cname":"new","name":"fallback.otherdomain.com"}}`)
+			return
+		}
+
+		w.WriteHeader(http.StatusNotFound)
+	}))
+	defer ts.Close()
+
+	logger := zerolog.Nop()
+	client, err := NewRESTClient(ts.URL, "account", "default-zone-from-login", "token", "agent", &logger)
+	assert.NoError(t, err)
+
+	tunnelID, _ := uuid.Parse("11111111-2222-3333-4444-555555555555")
+
+	t.Run("Success match", func(t *testing.T) {
+		route := NewDNSRoute("app.example.com", false)
+		res, err := client.RouteTunnel(tunnelID, route)
+		assert.NoError(t, err)
+		assert.NotNil(t, res)
+		assert.Equal(t, "Added CNAME app.example.com which will route to this tunnel", res.SuccessSummary())
+	})
+
+	t.Run("Fallback to default zone when no match", func(t *testing.T) {
+		route := NewDNSRoute("fallback.otherdomain.com", false)
+		res, err := client.RouteTunnel(tunnelID, route)
+		assert.NoError(t, err)
+		assert.NotNil(t, res)
+		assert.Equal(t, "Added CNAME fallback.otherdomain.com which will route to this tunnel", res.SuccessSummary())
+	})
+}