Mutualism between endogenous viruses and eukaryotes is still poorly understood.Whole genome data has highlighted the diverse distribution of viral sequences in several eukaryote host genomes. A group of endogenous double-stranded polydnaviruses known as bracoviruses has been identified in parasitic braconid wasp (Hymenoptera). Bracoviruses allow wasps to reproductively co-opt other insect larvae. Bracoviruses are excised from the host genome and injected in to the larva along side the wasp eggs; where they encode proteins that lower host immunity allowing development of parasitoid wasp larvae in the host. Interestingly, putative bracoviral sequences have recently been detected in the first sequenced genome of the tsetse fly (Diptera). This is peculiar since tsetse flies do not share this reproductive lifestyle. To investigate genome rearrangements associated with these unique mutual symbiotic relationships and examine its value as a potential vector control strategy entry point. We use comparative genomics to determine the presence, prevalence and genetic diversity of bracoviruses of five tsetse fly species (G. austeni, G. brevipalpis, G. f. fuscipes, G. m. morsitans and G. pallidipes) and the housefly (Musca domestica). We identify and use four viral Maverick genes as evolutionary models for bracoviruses. This is the first record of homologous bracoviruses in multiple Dipteran genomes. Phylogenetic reconstruction of each gene revealed two major clades that represent the two types of Mavericks. We detect varying magnitudes of purifying selection across these loci except for the poxvirus A32 gene, which is under positive selection. Moreover, these genes were inserted at conserved regions and co-evolve at similar rates with the host genomes.