We present evidence for the replacement of the typical type of mitochondrial (mt) genome of animals with a group of segments in the human body louse, Pediculus humanus. Unlike most other animals whose 37 mt genes are in a single ~15-kb DNA circle, mt genes of the human body louse are in at least 12 independent segments that are ~3 kb in size. Each segment has 1-3 genes and a large-non-coding region. All of the segments present in the human body louse are also present in the human head lice. Further, one segment that has the gene rrnS is also present in the human pubic louse and the langur louse. We found no evidence for the presence of any of these segments in the lice of chimpanzees, gorillas and lutungs. We infer that: (1) some of the mtDNA segments in the human body louse were present in the common ancestor of the lice of humans, other apes and the Old World monkeys, which lived ~22.5 million years ago (MYA); and (2) separated segments replaced the typical type of mt genome in the lineage that led to the human body louse after this lineage and the lineage that led to the chimpanzee louse diverged ~5.6 MYA. Increases in the proportion of separated segments may have been associated with founder events that apparently occurred in the lineage that led to the human body louse, and a selective advantage of these segments in replication over the typical type of mt genome.