Animal mitochondrial genomes (mitogenomes) typically exhibit a highly conserved gene content and organisation, with genes encoded on a single circular chromosome. However, many species of parasitic lice (Insecta: Phthiraptera) are notable exceptions, having mitogenomes fragmented into multiple circular chromosomes. To further understand the process of mitogenome fragmentation, we conducted a large-scale genomic study of a major group of lice, Amblycera. Using genomic information on mitogenome structure and a phylogenomic tree for 90 samples of this group, we found evidence for multiple independent origins of mitogenome fragmentation, some inferred to have occurred less than five million years ago. In addition, the base composition of mitogenomes in Amblycera shows less AT bias than other insects, and fragmentation is related to this reduction of AT bias. By combining phylogenomics and mitochondrial genomics, we provide a detailed portrait of mitogenome evolution across this major group of insects. The evidence of repeated and ongoing fragmentation represents a substantial advance in understanding the repeated nature of this process in lice.