Experimental approaches provide insight into the dynamics of species competition and coexistence, but studies of ectoparasitic arthropods are rare. Host choice experiments were undertaken in Amazonian Peru, by using obligate bat fly parasites of Seba’s short-tailed bat, Carollia perspicillata (L.). The fly species Trichobius joblingi Wenzel strongly preferred clean hosts to those previously infested with individuals of T. joblingi. Abundance thresholds may limit conspecific parasites on host individuals, and similar morphologies and habitat use may increase intraspecific competition among individuals of T. joblingi. T. joblingi did not distinguish between clean hosts and those previously infested with flies of another species, Speiseria ambigua Kessel. Results suggest that the presence of a morphologically dissimilar species does not preclude subsequent colonization. Differential microhabitat selection, aided by adaptive morphology, may facilitate species coexistence among ectoparasitic bat fly species.