Philopteridae feather lice are a group of ectoparasitic insects which have intimate relationships with their avian hosts. Feather lice include an enormous number of described species; however, the relationships of major lineages have been clouded by homoplasious characters due to convergent evolution. In this study, a comprehensive phylogenomic analysis of the group is performed which includes 137 feather louse species. Several other analyses are also completed including dating analysis, cophylogenetic reconstructions, and ancestral character estimation to understand the evolution of complex morphological and ecological traits. Phylogenetic results recover high support for the placement of major feather louse lineages, but with lower support for long-branched enigmatic genera found at the base of the tree. The results of dating analyses suggest modern feather lice began to diversify approximately 49 million years ago following the adaptive radiation of their avian hosts. Cost-based cophylogenetic reconstructions recover a high frequency of host switching, while congruence-based methods indicate a significant level of congruence between host and parasite trees. Ancestral state reconstructions favour a generalist ancestor and water bird host at the root. The analyses completed provide insight into the evolution of a diverse group of ectoparasitic insects which infest a wide variety of avian hosts. The results represent the most comprehensive phylogenetic hypothesis of the group to date and provide a framework for future classification of the family into natural groupings.