Abstract To gain a deeper understanding of the mechanisms affecting parasite gene dispersal and subsequent evolution, we investigated mitochondrial and nuclear DNA phylogeographic structures of two ectoparasitic louse species, Polyplax praomydis and Hoplopleura patersoni, and compared this to their host Micaelamys namaquensis. Analyses of mitochondrial and nuclear DNA sequence data derived from 13 geographic populations resulted in the detection of distinct phylogenetic clades within the parasite and host species. Strong support for host–parasite co-divergence was found over larger geographic scales but failed to show complete co-divergence over fine geographic scales. This finding led to the partial rejection of the hypothesis that the evolution of species-specific permanent parasites will mirror the phylogeographic pattern of their host. JANE co-phylogenetic reconstructions support the notion that host switching best explains the discrepancies in geographic patterns. We conclude that host specificity and permanency on the host only plays a partial role in maintaining co-divergences between parasites and their hosts.