diff --git a/CHANGELOG.md b/CHANGELOG.md
index 151406c0ac..0e35ec9549 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -99,6 +99,7 @@
 * [BUGFIX] Prevent panic at start if the http_prefix setting doesn't have a valid value. #3796
 * [BUGFIX] Memberlist: fixed panic caused by race condition in `armon/go-metrics` used by memberlist client. #3724
 * [BUGFIX] Querier: returning 422 (instead of 500) when query hits `max_chunks_per_query` limit with block storage. #3895
+* [BUGFIX] Alertmanager: Ensure that experimental `/api/v1/alerts` endpoints work when `-http.prefix` is empty. #3905
 
 ## 1.7.0
 
diff --git a/pkg/api/api.go b/pkg/api/api.go
index 989f7bca39..75177d83ce 100644
--- a/pkg/api/api.go
+++ b/pkg/api/api.go
@@ -172,19 +172,21 @@ func (a *API) RegisterAlertmanager(am *alertmanager.MultitenantAlertmanager, tar
 	a.RegisterRoutesWithPrefix(a.cfg.AlertmanagerHTTPPrefix, am, true)
 	level.Debug(a.logger).Log("msg", "api: registering alertmanager", "path_prefix", a.cfg.AlertmanagerHTTPPrefix)
 
-	// If the target is Alertmanager, enable the legacy behaviour. Otherwise only enable
-	// the component routed API.
-	if target {
-		a.RegisterRoute("/status", am.GetStatusHandler(), false, "GET")
-		a.RegisterRoutesWithPrefix(a.cfg.LegacyHTTPPrefix, am, true)
-	}
-
 	// MultiTenant Alertmanager Experimental API routes
 	if apiEnabled {
 		a.RegisterRoute("/api/v1/alerts", http.HandlerFunc(am.GetUserConfig), true, "GET")
 		a.RegisterRoute("/api/v1/alerts", http.HandlerFunc(am.SetUserConfig), true, "POST")
 		a.RegisterRoute("/api/v1/alerts", http.HandlerFunc(am.DeleteUserConfig), true, "DELETE")
 	}
+
+	// If the target is Alertmanager, enable the legacy behaviour. Otherwise only enable
+	// the component routed API.
+	if target {
+		a.RegisterRoute("/status", am.GetStatusHandler(), false, "GET")
+		// WARNING: If LegacyHTTPPrefix is an empty string, any other paths added after this point will be
+		// silently ignored by the HTTP service. Therefore, this must be the last route to be configured.
+		a.RegisterRoutesWithPrefix(a.cfg.LegacyHTTPPrefix, am, true)
+	}
 }
 
 // RegisterAPI registers the standard endpoints associated with a running Cortex.