Intraspecific brood parasitism is widespread among birds and provides clues for elucidating evolutionary origin of interspecific brood parasitism. Studies suggest that brood parasitism does not occur at random, but parasitic females select nests with advantages such as higher physical stability, reduced predation risk, or lower ectoparasite infestations. However, this evidence is sparse and mainly correlative. By experimentally increasing abundance of Carnus hemapterus (a common, generalist and widespread ectoparasitic nest-fly of a multitude of bird species) in half of the nests, we show that parasitic Spotless Starlings (Sturnus unicolor) avoid conspecific nests infested by ectoparasites. Since Carnus ectoparasites impinge costs on their avian nestling hosts, this avoidance response would be adaptive for parasitic starlings. Further, we suggest a mechanism by which parasite females may assess the level of ectoparasite infestation to select host nests accordingly: by using parasite cues such as faeces and blood remains. Additionally, these cues may be used by parasite females for synchronization with the reproductive cycle of host females because ectoparasite cues also indicate that incubation has already commenced. Whatever the functionality, the mechanism suggested here may be employed by intra-and interspecific brood parasites, so it might represent a widespread strategy in nature.