Host specificity of vectors is an important but understudied force shaping parasite evolution and the relationship between hosts and parasites. Low vector specificity may allow a vectored parasite to invade new host species, whereas high specificity of vectors may reduce the host range of the parasite and favor specialization. The ‘generalist’ and widely distributed avian skin mite Myialges caulotoon Speiser (Acari: Epidermoptidae) is unusual because females require an insect vector to complete their life cycle. Myialges caulotoon was previously reported from 2 lousefly (Diptera: Hippoboscidae) species, Olfersia sordida and Icosta nigra, parasitizing flightless cormorants (Phalacrocorax harrisi) and Galápagos hawks (Buteo galapagoensis), respectively, within the Galápagos Islands. This is a surprising distribution, given that the 2 lousefly species involved are relatively host-specific. Mitochondrial DNA sequences revealed 2 reciprocally monophyletic Myialges clades that sorted out perfectly with respect to their vector species, regardless of whether they were in allopatry or sympatry. One clade was restricted to flies of hawks and the other to flies of cormorants. Females of the 2 Myialges groups were also separated consistently by the shape of the sternal surface sclerotization. Mites of hawk flies were more abundant than those of cormorant flies. Within the Myialges clade associated with hawks, genetic differentiation between 2 island populations mirrored its host's patterns of differentiation.