The genus Cypsharpirhynchus Fain, 1995 (Acariformes: Harpirhynchidae: Harpirhynchinae) is lowered in the rank to the subgenus of the genus Harpyrhynchiella Fain, 1972 based on the examination of the external morphology in both sexes. The revised diagnoses of the genus Harpirhynchiella and its subgenera are provided. A new species, Harpyrhynchiella (Cypsharpirhynchus) apus sp. nov., is described from both sexes ex Apus apus (Linnaeus, 1758) (Apodiformes: Apodidae) in the northwest of Russia. Females of the new species differ from Harpyrhynchiella (Cypsharpirhynchus) cypsiuri Fain, 1972 by the longer body (380-400) (versus 285-320 in H. cypsiuri), the presence of the accessory dorsal shields (versus absence) and by the lateral tuberculate areas that do not reach close to the lateral margins of the idiosoma (versus reaching). Notes on mating strategy of these mites are provided. Some larvae (designated female larvae) of Harpyrhynchiella apus have an internal, globular, sclerotized structure presumed to be a spermatheca, while others (designated male larvae) lack this structure. This is the first record of such sexual dimorphism in larvae of Harpirhynchidae. In Harpyrhynchiella spp., almost immobile female nymphs and adult females live individually in intracutaneous layers; females remain within the nymphal skin and oviposit there. This life history suggests that mating takes place on the skin between adult males and female larvae. The inseminated larva burrows into the host skin and moults there into the immobile female nymph or the female larva moults on the host skin surface and the weakly mobile nymph burrows into the skin.