Whereas the mitochondrial genomes of most animals consist of a single circular chromosome, the mitochondrial genes of several species of parasitic lice (Insecta: Phthiraptera) are separated on multiple circular fragments. This phenomenon has arisen at least 12 times within lice and is present in all major groups of lice. However, very little is known about evolutionary causes and consequences of mitogenome fragmentation in these insects. Here we use whole genome sequence data to test 1) the phylogenetic scale of mitogenome fragmentation and 2) hypotheses regarding the evolutionary mechanisms behind fragmentation. Specifically, we compared mitogenomes at different phylogenetic scales within parasitic lice. We then compared nucleotide composition and signatures of selection among different mitogenomes. From these comparisons, we found that patterns of mitogenome fragmentation tend to be consistent with phylogenetic scale: they are not conserved across the phylogeny of lice, are more conserved within clades, and are highly conserved within genera and species. However, there were differences in gene order even among individuals of the same species, suggesting mitogenome architecture changes frequently and rapidly within lice. Nucleotide composition varied considerably among the mitogenomes. Notably, AT% was significantly lower in fragmented mitogenomes, which could be related to fewer deamination mutations due to a shorter genome replication time. There was also variation in the signal of selection among different mitogenomes, suggesting that fragmentation is not a neutral process in lice. Overall, this study helps to provide an essential evolutionary framework for assessing the mechanisms driving the complexity of louse mitogenomes.