Parasite dispersal can shape host-parasite interactions at both deep and shallow timescales. One approach to understanding the effects of dispersal is to study parasite lineages that differ in dispersal capability but are from the same group of hosts. We compared phylogenetic and population genetic patterns of wing and body lice from ground-doves. Wing lice are more capable of dispersal than body lice. We sequenced full genomes of individual lice for multiple representatives of several wing and body louse species. From these data, we assembled genes for phylogenetic analysis and called SNPs for population genetic analysis. At the phylogenetic level, body lice showed more codivergence with their hosts than did wing lice. However, both wing and body lice exhibited some phylogenetic congruence with their hosts. Within species, body lice showed more population genetic structure than wing lice, although both types of lice showed some structure according to biogeography. Body lice also had significantly lower heterozygosity than wing lice, suggesting more inbreeding. Our results demonstrate that dispersal can shape a host-parasite system across evolutionary time, but also that other factors (e.g., host association and biogeography) can have varying degrees of influence on different groups of parasites and at different timescales.