Cynocephalid dermopterans (flying lemurs) are represented by only two living genera (Cynocephalus and Galeopterus), which inhabit tropical rainforests of South‐East Asia. Despite their very poor diversity and their limited distribution, dermopterans play a critical role in higher‐level eutherian phylogeny inasmuch as they represent together with Scandentia (tree‐shrew) the sister group of the Primates clade (Plesiadapiformes + Euprimates). However, unlike primates, for which the fossil record extends back to the early Palaeogene on all Holarctic continents and in Africa, the evolutionary history of the order Dermoptera sensu stricto (Cynocephalidae) has so far remained undocumented, with the exception of a badly preserved fragment of mandible from the late Eocene of Thailand (Dermotherium major). In this paper, we described newly discovered fossil dermopterans (essentially dental remains) from different regions of South Asia (Thailand, Myanmar, and Pakistan) ranging from the late middle Eocene to the late Oligocene. We performed microtomographic examinations at the European Synchrotron Radiation Facility (ESRF, Grenoble, France) to analyse different morphological aspects of the fossilized jaws. The abundant material from the late Oligocene of Thailand (Nong Ya Plong coal mine) allows us to emend the diagnosis of the genus Dermotherium and to describe a new species: Dermotherium chimaera sp. n. This species exhibits an interesting mosaic of plesiomorphic cynocephalid characters shared with Cynocephalus and Galeopterus, and as such, it probably documents a form close to the ancestral morphotype from which the two extant forms are derived (supported by cladistic assessment of the dental evidence). The discovery of Palaeogene cynocephalids is particularly significant since it attests to the great antiquity of the order Dermoptera in Asia, and besides, it provides the first spatio‐temporal glimpse into the evolutionary history of that enigmatic mammal group. In that respect, these fossils testify to a long history of endemism in South Asia for dermopterans, and demonstrate that their modern geographic restriction in south‐eastern Asia is clearly a relictual distribution. Cynocephalids had a more widespread distribution during the Palaeogene, which extended from the Indian subcontinent (the rafting Greater India) to South‐East Asia. Their subsequent extinction on the Indian subcontinent was probably mediated by the major palaeogeographic and geomorphologic events related to the India‐Eurasia collision (retreat of the Paratethys Sea, formation of orogenic highlands) that have strongly affected the climate of South Asia at the end of the Oligocene.