The aardwolf (Proteles cristata) is a unique, insectivorous species of the family Hyaenidae. It occupies a disjunct range in eastern and southern Africa and is possibly a remaining member of a historical dog-like hyaena clade. Although both local and global population status and trends are largely unknown, aardwolves are not uncommon in arid grasslands and the IUCN conservation status of Least Concern appears to be justified. However, they are one of the least studied of the four hyaena species, and we have scarce information about the genetic structure of aardwolf populations. Here, we present the first complete aardwolf mitochondrial genomes and provide novel information about aardwolf evolutionary origins and genetic structure within a single population. Through the investigation of complete mitochondrial genomes from five individuals from a single population within South Africa, we find the mitochondrial diversity of this population to be neither particularly high nor low compared to a number of other mammalian species. Moreover, we also provide additional evidence towards the basal position of the aardwolf within Hyaenidae with a divergence time of 13.0 Ma (95% CI 10.1–16.4 Ma) from all other extant hyaena species.