diff --git a/docs/pages/enroll-resources/application-access/guides/connecting-apps.mdx b/docs/pages/enroll-resources/application-access/guides/connecting-apps.mdx
index 48aea459dd71f..0fdc2f93776f1 100644
--- a/docs/pages/enroll-resources/application-access/guides/connecting-apps.mdx
+++ b/docs/pages/enroll-resources/application-access/guides/connecting-apps.mdx
@@ -17,7 +17,7 @@ Application Service, which uses a join token to establish trust with the
 Teleport Auth Service. Users visit Teleport-protected web applications through
 the Teleport Web UI. The Teleport Proxy Service routes browser traffic to the
 Teleport Application Service, which forwards HTTP requests to and from target
-applications. 
+applications.
 
 ## Prerequisites
 
@@ -38,7 +38,7 @@ target application, then deploy a Teleport Agent to run the service.
 ### Generate a token
 
 A join token is required to authorize a Teleport Application Service to
-join the cluster. 
+join the cluster.
 
 1. Generate a short-lived join token. Make sure to change `app-name` to the name
    of your application and `app-uri` to the application's domain name and port:
@@ -195,6 +195,7 @@ address. To override the public address, specify the `public_addr` field:
 ```yaml
 - name: "jira"
   uri: "https://localhost:8001"
+  # The public address must be a unique DNS name and not conflict with the Teleport cluster's public addresses.
   public_addr: "jira.example.com"
 ```
 
diff --git a/lib/auth/grpcserver.go b/lib/auth/grpcserver.go
index 247d2b76a0ca0..e4acacc53889e 100644
--- a/lib/auth/grpcserver.go
+++ b/lib/auth/grpcserver.go
@@ -1489,6 +1489,10 @@ func (g *GRPCServer) UpsertApplicationServer(ctx context.Context, req *authpb.Up
 		}
 	}
 
+	if err := services.ValidateApp(app, auth); err != nil {
+		return nil, trace.Wrap(err)
+	}
+
 	keepAlive, err := auth.UpsertApplicationServer(ctx, server)
 	if err != nil {
 		return nil, trace.Wrap(err)
@@ -3846,6 +3850,9 @@ func (g *GRPCServer) CreateApp(ctx context.Context, app *types.AppV3) (*emptypb.
 	if app.Origin() == "" {
 		app.SetOrigin(types.OriginDynamic)
 	}
+	if err := services.ValidateApp(app, auth); err != nil {
+		return nil, trace.Wrap(err)
+	}
 	if err := auth.CreateApp(ctx, app); err != nil {
 		return nil, trace.Wrap(err)
 	}
@@ -3861,6 +3868,9 @@ func (g *GRPCServer) UpdateApp(ctx context.Context, app *types.AppV3) (*emptypb.
 	if app.Origin() == "" {
 		app.SetOrigin(types.OriginDynamic)
 	}
+	if err := services.ValidateApp(app, auth); err != nil {
+		return nil, trace.Wrap(err)
+	}
 	if err := auth.UpdateApp(ctx, app); err != nil {
 		return nil, trace.Wrap(err)
 	}
diff --git a/lib/auth/grpcserver_test.go b/lib/auth/grpcserver_test.go
index 05642d00aa3c9..fc1caeb87f5b6 100644
--- a/lib/auth/grpcserver_test.go
+++ b/lib/auth/grpcserver_test.go
@@ -3680,6 +3680,45 @@ func TestAppsCRUD(t *testing.T) {
 		iterOut = append(iterOut, app)
 	}
 	require.Empty(t, iterOut)
+
+	err = srv.Auth().UpsertProxy(ctx, &types.ServerV2{
+		Kind: types.KindProxy,
+		Metadata: types.Metadata{
+			Name: "proxy",
+		},
+		Spec: types.ServerSpecV2{
+			PublicAddrs: []string{"proxy.example.com:443"},
+		},
+	})
+	require.NoError(t, err)
+
+	t.Run("Creating an app with a public address matching a proxy address should fail", func(t *testing.T) {
+		misconfiguredApp, err := types.NewAppV3(types.Metadata{
+			Name:   "misconfigured-app",
+			Labels: map[string]string{types.OriginLabel: types.OriginDynamic},
+		}, types.AppSpecV3{
+			URI:        "localhost1",
+			PublicAddr: "proxy.example.com",
+		})
+		require.NoError(t, err)
+
+		err = clt.CreateApp(ctx, misconfiguredApp)
+		require.ErrorIs(t, err, trace.BadParameter(`Application "misconfigured-app" public address "proxy.example.com" conflicts with the Teleport Proxy public address. Configure the application to use a unique public address that does not match the proxy's public addresses. Refer to https://goteleport.com/docs/enroll-resources/application-access/guides/connecting-apps/.`))
+	})
+
+	t.Run("Updating an app with a public address matching a proxy address should fail", func(t *testing.T) {
+		misconfiguredApp, err := types.NewAppV3(types.Metadata{
+			Name:   "misconfigured-app",
+			Labels: map[string]string{types.OriginLabel: types.OriginDynamic},
+		}, types.AppSpecV3{
+			URI:        "localhost1",
+			PublicAddr: "proxy.example.com",
+		})
+		require.NoError(t, err)
+
+		err = clt.UpdateApp(ctx, misconfiguredApp)
+		require.ErrorIs(t, err, trace.BadParameter(`Application "misconfigured-app" public address "proxy.example.com" conflicts with the Teleport Proxy public address. Configure the application to use a unique public address that does not match the proxy's public addresses. Refer to https://goteleport.com/docs/enroll-resources/application-access/guides/connecting-apps/.`))
+	})
 }
 
 // TestAppServersCRUD tests application server resource operations.
@@ -3778,6 +3817,34 @@ func TestAppServersCRUD(t *testing.T) {
 	})
 	require.NoError(t, err)
 	require.Empty(t, resources.Resources)
+
+	t.Run("App server with an app that has a public address matching a proxy address should fail", func(t *testing.T) {
+		err = srv.Auth().UpsertProxy(ctx, &types.ServerV2{
+			Kind: types.KindProxy,
+			Metadata: types.Metadata{
+				Name: "proxy",
+			},
+			Spec: types.ServerSpecV2{
+				PublicAddrs: []string{"proxy.example.com:443"},
+			},
+		})
+		require.NoError(t, err)
+
+		misconfiguredApp, err := types.NewAppV3(types.Metadata{
+			Name:   "misconfigured-app",
+			Labels: map[string]string{types.OriginLabel: types.OriginDynamic},
+		}, types.AppSpecV3{
+			URI:        "localhost1",
+			PublicAddr: "proxy.example.com",
+		})
+		require.NoError(t, err)
+
+		appServer, err := types.NewAppServerV3FromApp(misconfiguredApp, "misconfigured-app", "hostID")
+		require.NoError(t, err)
+
+		_, err = clt.UpsertApplicationServer(ctx, appServer)
+		require.ErrorIs(t, err, trace.BadParameter(`Application "misconfigured-app" public address "proxy.example.com" conflicts with the Teleport Proxy public address. Configure the application to use a unique public address that does not match the proxy's public addresses. Refer to https://goteleport.com/docs/enroll-resources/application-access/guides/connecting-apps/.`))
+	})
 }
 
 // TestDatabasesCRUD tests database resource operations.
diff --git a/lib/service/service.go b/lib/service/service.go
index 143725678eadd..518af0b988a3c 100644
--- a/lib/service/service.go
+++ b/lib/service/service.go
@@ -6402,6 +6402,10 @@ func (process *TeleportProcess) initApps() {
 				return trace.Wrap(err)
 			}
 
+			if err := services.ValidateApp(a, accessPoint); err != nil {
+				return trace.Wrap(err)
+			}
+
 			applications = append(applications, a)
 		}
 
diff --git a/lib/services/app.go b/lib/services/app.go
index 096d136000b8c..dbd970edc06de 100644
--- a/lib/services/app.go
+++ b/lib/services/app.go
@@ -25,6 +25,7 @@ import (
 	"net"
 	"net/url"
 	"os"
+	"slices"
 	"strconv"
 	"strings"
 	"sync"
@@ -64,6 +65,43 @@ type Applications interface {
 	DeleteAllApps(context.Context) error
 }
 
+// ValidateApp validates the Application resource.
+func ValidateApp(app types.Application, proxyGetter ProxyGetter) error {
+	// Prevent routing conflicts and session hijacking by ensuring the application's public address does not match the
+	// public address of any proxy. If an application shares a public address with a proxy, requests intended for the
+	// proxy could be misrouted to the application, compromising security.
+	if app.GetPublicAddr() != "" {
+		proxyServers, err := proxyGetter.GetProxies()
+		if err != nil {
+			return trace.Wrap(err)
+		}
+
+		for _, proxyServer := range proxyServers {
+			proxyAddrs, err := utils.ParseAddrs(proxyServer.GetPublicAddrs())
+			if err != nil {
+				return trace.Wrap(err)
+			}
+
+			if slices.ContainsFunc(
+				proxyAddrs,
+				func(proxyAddr utils.NetAddr) bool {
+					return app.GetPublicAddr() == proxyAddr.Host()
+				},
+			) {
+				return trace.BadParameter(
+					"Application %q public address %q conflicts with the Teleport Proxy public address. "+
+						"Configure the application to use a unique public address that does not match the proxy's public addresses. "+
+						"Refer to https://goteleport.com/docs/enroll-resources/application-access/guides/connecting-apps/.",
+					app.GetName(),
+					app.GetPublicAddr(),
+				)
+			}
+		}
+	}
+
+	return nil
+}
+
 // MarshalApp marshals Application resource to JSON.
 func MarshalApp(app types.Application, opts ...MarshalOption) ([]byte, error) {
 	cfg, err := CollectOptions(opts)
diff --git a/lib/services/app_test.go b/lib/services/app_test.go
index 2dadd3fdb6cf6..65b58133f1282 100644
--- a/lib/services/app_test.go
+++ b/lib/services/app_test.go
@@ -29,6 +29,83 @@ import (
 	"github.com/gravitational/teleport/lib/utils"
 )
 
+func TestValidateApp(t *testing.T) {
+	tests := []struct {
+		name       string
+		app        types.Application
+		proxyAddrs []string
+		wantErr    string
+	}{
+		{
+			name: "no public addr, no error",
+			app: func() types.Application {
+				app, _ := types.NewAppV3(types.Metadata{Name: "app"}, types.AppSpecV3{URI: "http://localhost:8080"})
+				return app
+			}(),
+			proxyAddrs: []string{"web.example.com:443"},
+		},
+		{
+			name: "public addr does not conflict",
+			app: func() types.Application {
+				app, _ := types.NewAppV3(types.Metadata{Name: "app"}, types.AppSpecV3{URI: "http://localhost:8080", PublicAddr: "app.example.com"})
+				return app
+			}(),
+			proxyAddrs: []string{"web.example.com:443"},
+		},
+		{
+			name: "public addr matches proxy host",
+			app: func() types.Application {
+				app, _ := types.NewAppV3(types.Metadata{Name: "app"}, types.AppSpecV3{URI: "http://localhost:8080", PublicAddr: "web.example.com"})
+				return app
+			}(),
+			proxyAddrs: []string{"web.example.com:443"},
+			wantErr:    "conflicts with the Teleport Proxy public address",
+		},
+		{
+			name: "multiple proxy addrs, one matches",
+			app: func() types.Application {
+				app, _ := types.NewAppV3(types.Metadata{Name: "app"}, types.AppSpecV3{URI: "http://localhost:8080", PublicAddr: "web.example.com"})
+				return app
+			}(),
+			proxyAddrs: []string{"other.com:443", "web.example.com:443"},
+			wantErr:    "conflicts with the Teleport Proxy public address",
+		},
+	}
+
+	for _, tt := range tests {
+		t.Run(tt.name, func(t *testing.T) {
+			err := ValidateApp(tt.app, &mockProxyGetter{addrs: tt.proxyAddrs})
+			if tt.wantErr != "" {
+				require.ErrorContains(t, err, tt.wantErr)
+			} else {
+				require.NoError(t, err)
+			}
+		})
+	}
+}
+
+// mockProxyGetter is a test implementation of ProxyGetter.
+type mockProxyGetter struct {
+	addrs []string
+}
+
+func (m *mockProxyGetter) GetProxies() ([]types.Server, error) {
+	servers := make([]types.Server, 0, len(m.addrs))
+
+	for _, addr := range m.addrs {
+		servers = append(
+			servers,
+			&types.ServerV2{
+				Spec: types.ServerSpecV2{
+					PublicAddrs: []string{addr},
+				},
+			},
+		)
+	}
+
+	return servers, nil
+}
+
 // TestApplicationUnmarshal verifies an app resource can be unmarshaled.
 func TestApplicationUnmarshal(t *testing.T) {
 	expected, err := types.NewAppV3(types.Metadata{
diff --git a/lib/web/app/middleware.go b/lib/web/app/middleware.go
index 2d364e8bc109e..71bf21020b15b 100644
--- a/lib/web/app/middleware.go
+++ b/lib/web/app/middleware.go
@@ -73,13 +73,15 @@ func (h *Handler) redirectToLauncher(w http.ResponseWriter, r *http.Request, p l
 	}
 
 	if h.c.WebPublicAddr == "" {
-		// The error below tends to be swallowed by the Web UI, so log a warning for
-		// admins as well.
-		const msg = "Application Service requires public_addr to be set in the Teleport Proxy Service configuration. " +
-			"Please contact your Teleport cluster administrator or refer to " +
-			"https://goteleport.com/docs/enroll-resources/application-access/guides/connecting-apps/."
-		h.logger.ErrorContext(r.Context(), msg)
-		return trace.BadParameter("public address of the proxy is not set")
+		const errMsg = "Application Service requires public_addr to be set in the Teleport Proxy Service configuration. " +
+			"Update the Teleport Proxy Service configuration to include a public_addr. " +
+			"Refer to https://goteleport.com/docs/enroll-resources/application-access/guides/connecting-apps/."
+
+		// Log the error to warn admins 🚩
+		h.logger.ErrorContext(r.Context(), errMsg)
+
+		// Immediately return an error since this is a critical misconfiguration 🛑
+		return trace.BadParameter(errMsg)
 	}
 
 	addr, err := utils.ParseAddr(r.Host)
@@ -87,11 +89,26 @@ func (h *Handler) redirectToLauncher(w http.ResponseWriter, r *http.Request, p l
 		return trace.Wrap(err)
 	}
 
-	var proxyPublicAddrs []string
+	proxyPublicAddrs := make([]string, 0, len(h.c.ProxyPublicAddrs))
+
 	for _, proxyAddr := range h.c.ProxyPublicAddrs {
-		// preserving full `host:port` to support proxy hosted on non-standard HTTPS port.
+		if p.publicAddr == proxyAddr.Host() {
+			const errMsg = "Application public address conflicts with the Teleport Proxy public address. " +
+				"Configure the application to use a unique public address that does not match the proxy's public addresses. " +
+				"Refer to https://goteleport.com/docs/enroll-resources/application-access/guides/connecting-apps/."
+
+			// Log the error to warn admins 🚩
+			h.logger.ErrorContext(r.Context(), errMsg, "launcher_params", p)
+
+			// Immediately return an error since this is a critical misconfiguration 🛑
+			return trace.BadParameter(errMsg)
+		}
+
+		// Append the full proxy address (host:port) to the list, preserving the port information.
+		// This is necessary to support proxies running on non-standard HTTPS ports and ensure accurate DNS matching.
 		proxyPublicAddrs = append(proxyPublicAddrs, proxyAddr.String())
 	}
+
 	proxyDNSName := utils.FindMatchingProxyDNS(r.Host, proxyPublicAddrs)
 	urlString := makeAppRedirectURL(r, proxyDNSName, addr.Host(), p)
 	http.Redirect(w, r, urlString, http.StatusFound)
@@ -122,7 +139,7 @@ func makeHandler(handler handlerFunc) http.HandlerFunc {
 // response writer.
 func writeError(w http.ResponseWriter, err error) {
 	code := trace.ErrorToCode(err)
-	http.Error(w, http.StatusText(code), code)
+	http.Error(w, err.Error(), code)
 }
 
 type routerFunc func(http.ResponseWriter, *http.Request, httprouter.Params) error