Whereas a majority of monogenean flatworms are ectoparasitic, i.e., parasitize on external surfaces (mainly gills) of their fish hosts, Enterogyrus species (subfamily Ancyrocephalinae) are mesoparasitic, i.e., parasitize in the stomach of the host. As there are numerous drastic differences between these two environments (including lower oxygen availability), we hypothesized that this life-history innovation might have produced adaptive pressures on the energy metabolism, which is partially encoded by the mitochondrial genome (OXPHOS). To test this hypothesis, we sequenced mitochondrial genomes of two Ancyrocephalinae species: mesoparasitic E. malmbergi and ectoparasitic Ancyrocephalus mogurndae. The mitogenomic architecture of E. malmbergi is mostly standard for monogeneans, but that of A. mogurndae exhibits some unique features: missing trnL2 gene, very low AT content (60%), a non-canonical start codon of the nad2 gene, and exceptionally long tandem-repeats in the non-coding region (253 bp). Phylogenetic analyses produced paraphyletic Ancyrocephalinae (with embedded Dactylogyrinae), but with low support values. Selective pressure (PAML and HYPHY) and protein structure analyses all found evidence for adaptive evolution in cox2 and cox3 genes of the mesoparasitic E. malmbergi. These findings tentatively support our hypothesis of adaptive evolution driven by life-history innovations in the mitogenome of this species. However, as only one stomach-inhabiting mesoparasitic monogenean was available for this analysis, our findings should be corroborated on a larger number of mesoparasitic monogeneans and by physiological studies.