The systematics of the arid-adapted Old World Gerbillus rodent genus has always been challenging, with many different taxonomic arrangements proposed. Beyond such taxonomic aspects, the timing and geographical pattern of the evolutionary history of this group remains largely unknown. Based on mitochondrial (cytochrome b) and nuclear (interphotoreceptor retinoid-binding protein) sequences obtained from the specimens of 21 species, we conducted a phylogenetic analysis of the group, estimated the ages and putative ancestral ranges of its major lineages. Four major clades were clearly retrieved within Gerbillus, for which we propose a subgenus rank. We showed that the emergence of the genus dates back to the end of the Miocene, which corresponds to a period of aridification and C4 vegetation expansion in open habitats, while the four sublineages originated at the end of the Pliocene. Most subsequent diversification events occurred during the Pleistocene, a period characterized by recurrent climatic/environmental shifts with increasing aridification during the last two millions of years. Finally, we suggested that most of the Gerbillus evolutionary history took place in Africa. Only in a few instances did dispersal events from Africa to Asia give birth to extant Asian lineages, a pattern that contrasts with what has been found in many animal groups.