Pteropus is the most speciose genus in Pteropodidae, currently comprising 65 species in 18 species groups. Here we examine whether Pteropus as currently understood is monophyletic. We sequenced three nuclear genes (RAG-1, RAG-2 and vWF) totalling c. 3.0 kbp from 18 species of Pteropus representing 12 species groups, plus Acerodon celebensis and megachiropteran outgroups representing all other subfamilies and tribes. Separate and combined parsimony and maximum likelihood analyses recovered a clade containing Acerodon as sister to all Pteropus species to the exclusion of the Philippine endemic taxon ‘P. leucopterus’, rendering Pteropus paraphyletic. We propose the revalidation of Desmalopex Miller, 1907, an available generic name for leucopterus, adopting the name combination Desmalopex leucopterus (Temminck, 1853). We discuss implications of this result and anticipate further modifications of the classification of Pteropus.