Competition-colonization trade-off models explain the coexistence of competing species in terms of a trade-off between competitive ability and the ability to colonize competitor-free patches of habitat. A simple prediction of these models is that inferior competitors will be superior dispersers. This prediction has seldom been tested in natural populations because measuring dispersal is difficult. Host-parasite systems are promising in this regard, especially those involving "permanent" parasites that complete their entire life cycle on the body of the host. Because of this close association with the host, the dispersal, i.e., transmission, of these parasites can be monitored very accurately. We tested the dispersal prediction of the competition-colonization model by documenting the transmission dynamics of feather-feeding lice, which are permanent, relatively host-specific parasites of birds. We compared two groups known as "wing" lice and "body" lice that are common parasites of Rock Pigeons (Columba livia Gmelin). The two groups are ecologically similar, and they compete for resources on the host. Previous work shows that body lice are competitively superior to wing lice, leading us to predict that wing lice should be better than body lice at dispersing to new host individuals. We tested this prediction by comparing the ability of wing and body lice to disperse between hosts using vertical- and horizontal-transmission mechanisms, including phoretic hitchhiking on parasitic flies (Diptera: Hippoboscidae). A series of experiments with both captive and wild birds confirmed that wing lice are much better than body lice at colonizing new hosts. Wing lice showed significantly greater vertical transmission to nestlings, and they were quite capable of phoretic transmission to new hosts on flies. In contrast, body lice were not phoretic. These results provide the first rigorous demonstration of phoretic transmission in lice, and they underscore the importance of a community-level approach to understanding the ecology of parasite transmission dynamics.