The bat skin mites from the closely-related Demodecidae and Psorergatidae families occur synhospitally, populating the same host species and perhaps neighboring microhabitats. However, data on their occurrence and parasitism are fragmentary and dispersed. Thus far, 27 Demodecidae and 18 Psorergatidae species have been described, but the coexistence of mites from both families was only demonstrated in six species of bats. This article presents a description of Demodex pusillus sp. nov. from Nyctalus noctula, including a new host record (first observation of demodecid mites in Nyctalus) and a new record concerning the occurrence of Psorergatoides kerivoluae in Plecotus auritus. It also includes an updated global checklist of the occurrence of Demodecidae and Psorergatidae in Chiroptera, including data on their records/distribution and location in their hosts. In both studied families, the mites exhibit preferences, and even topographic specificity, colonizing different microhabitats in the host, including the eye region (e.g., Meibomian glands of the eyes, corneal surface and eyelid vault), wing membranes and hairy skin on the body. Such colonization of separate microhabitats enables different species to co-occur within the same host, while the total number of parasites determines the level of parasite load, with higher levels being associated with the incidence of disease symptoms. It is worth mentioning that Demodex pusillus sp. nov. is the smallest known representative of the Demodecidae family and one of the smallest animals (70–80 micrometers in length).