Feather lice (Phthiraptera: Ischnocera) have long been known to hitchhike rides on parasitic louse flies (Diptera: Hippoboscidae). Since louse flies are less host-specific than lice, this fascinating behavior may play an important role in host switching by lice. Indeed, differences in rates of phoresis could explain differences in the overall coevolutionary patterns of different groups of lice. For example “body” lice of pigeons and doves exhibit greater host specificity, population genetic structure, and co-phylogenetic congruence, than do “wing” lice on the same hosts. These differences are intriguing because the two groups of lice feed on identical feathers, have similar life cycles, and have similar fitness when transferred experimentally to novel species of pigeons and doves. We conducted an experiment using captive Rock Pigeons (Columba livia) to compare rates of phoresis by wing and body lice on pigeon flies (Pseudolynchia canariensis). Our results show conclusively that wing lice move between individual pigeons, and between pigeons and Mourning Doves (Zenaida macroura), by hitchhiking on flies, whereas body lice are not phoretic. Dispersal to Mourning Doves by wing lice represents an experimental host switch because wing lice do not normally occur on this species. Laboratory experiments further show that wing lice are better than body lice at remaining attached to flies that are walking, flying, or grooming; these differences may explain why wing lice are phoretic, while body lice are not. In conclusion, our results confirm a possible role for phoretic hitchhiking in shaping coevolutionary patterns and processes.