Many parasitic insects, including lice, form close relationships with endosymbiotic bacteria that are crucial for their survival. In this study, we used genomic sequencing to investigate the distribution and evolutionary history of the bacterial genus Sodalis across a broad range of feather louse species spanning 156 genera. Phylogenomic analysis revealed significant diversity among Sodalis lineages in feather lice, and robust evidence for their independent and repeated acquisition by different louse clades throughout their radiation. Among the 1,020 louse genomes analyzed, at least 22% contained Sodalis, distributed across 57 louse genera. Cophylogenetic analyses between the Sodalis and feather louse phylogenies indicated considerable mismatch. This phylogenetic incongruence between lice and Sodalis, along with the presence of distantly related Sodalis lineages in otherwise closely related louse species, strongly indicates repeated independent acquisition of this endosymbiont. Additionally, evidence of cospeciation among a few closely related louse species, coupled with frequent acquisition of these endosymbionts from free-living bacteria, further highlights the diverse evolutionary processes shaping Sodalis endosymbiosis in feather lice.