Andrya arctica is a cestode parasite of the family Anoplocephalidae (Cyclophyllidea), parasitizing lemmings of the genus Dicrostonyx throughout the Holarctic region. The population structure of this intestinal parasite was studied from eight different regions, six of which represented different genetic entities of lemming hosts. Molecular sequence tagged site markers and minisatellite fingerprints as well as morphology and morphometries were used to reveal the population structure of A. arctica in the Holarctic region. The results suggest that the evolutionary history of this cestode species has included different processes acting on different geographical regions. On the Siberian mainland (host D. torquatus), the division of the parasites into different genetic entities agreed perfectly with the chromosomal races of the lemming hosts that points towards a shared evolutionary history between the host and the parasite (‘cospeciation’). The main phylogenetic split of Dicrostonyx between Eurasia and North America was not, however, observed in A. arctica. This suggests that in the Nearctic (host D. groenlandicus) the parasite has remained relatively unmodified because of the large cohesive populations (‘coadaptation’). The uniqueness of the Greenland population, and possibly also that of the Wrangel Island, can be explained by peripheral isolation, refugial effects or founder effects.