diff --git a/platform-api/internal/server/overrides.go b/platform-api/internal/server/overrides.go
index 62cc2f7bc3..3d85e06d84 100644
--- a/platform-api/internal/server/overrides.go
+++ b/platform-api/internal/server/overrides.go
@@ -22,6 +22,7 @@ import (
 	"log/slog"
 	"net/http"
 	"sort"
+	"strings"
 
 	"github.com/wso2/api-platform/platform-api/internal/router"
 )
@@ -56,10 +57,12 @@ func installCoreRoutes(
 	}
 	if len(unknown) > 0 {
 		sort.Strings(unknown)
-		p := unknown[0]
-		return fmt.Errorf("plugin %q declared a route override for %q, which is not a core route "+
-			"(patterns are matched exactly, including method and path; %d override(s) unmatched)",
-			overrides[p].plugin, p, len(unknown))
+		claims := make([]string, 0, len(unknown))
+		for _, pattern := range unknown {
+			claims = append(claims, fmt.Sprintf("plugin %q -> %q", overrides[pattern].plugin, pattern))
+		}
+		return fmt.Errorf("%d route override(s) name a pattern that is not a core route: %s",
+			len(unknown), strings.Join(claims, "; "))
 	}
 
 	// A duplicate pattern can now only come from a plugin route registered on
diff --git a/platform-api/internal/server/overrides_test.go b/platform-api/internal/server/overrides_test.go
index f3900fafb0..171145f66d 100644
--- a/platform-api/internal/server/overrides_test.go
+++ b/platform-api/internal/server/overrides_test.go
@@ -301,6 +301,38 @@ func TestInstallCoreRoutes_UnknownPatternAbortsStartup(t *testing.T) {
 	}
 }
 
+// One unmatched pattern per error would mean fixing a typo, restarting, and
+// finding the next one — so the error names every unmatched override at once,
+// each paired with the plugin that claimed it and ordered by pattern. The whole
+// message is compared: a claim listing the wrong plugin, or claims in map order,
+// is exactly what the operator reading it cannot afford.
+func TestInstallCoreRoutes_UnknownPatternErrorNamesEveryOverride(t *testing.T) {
+	cloud := &overridePlugin{
+		fakePlugin: &fakePlugin{name: "cloud", spec: specWithScopes},
+		overrides: []pdk.RouteOverride{
+			{Pattern: "GET /api/v1/gateways/{gatewayId}", Wrap: passthrough},
+			{Pattern: "GET /api/v0.9/gateways/{id}", Wrap: passthrough},
+		},
+	}
+	audit := &overridePlugin{
+		fakePlugin: &fakePlugin{name: "audit", spec: specWithScopes},
+		overrides:  []pdk.RouteOverride{{Pattern: "POST /api/v0.9/gateways", Wrap: passthrough}},
+	}
+
+	_, err := startup(t, coreRecorder(map[string]int{}), cloud, audit)
+	if err == nil {
+		t.Fatal("expected startup to abort, got nil error")
+	}
+
+	want := `3 route override(s) name a pattern that is not a core route: ` +
+		`plugin "cloud" -> "GET /api/v0.9/gateways/{id}"; ` +
+		`plugin "cloud" -> "GET /api/v1/gateways/{gatewayId}"; ` +
+		`plugin "audit" -> "POST /api/v0.9/gateways"`
+	if err.Error() != want {
+		t.Fatalf("error message mismatch\n got: %s\nwant: %s", err.Error(), want)
+	}
+}
+
 // Two decorators on one route would have to be ordered by something no plugin
 // author can see, so this is a startup error naming both claimants.
 func TestInitPlugins_TwoPluginsClaimingOnePatternAbortStartup(t *testing.T) {