The subfamily Murininae is renowned for its inherent taxonomic challenges associated with sampling difficulties and morphological similarities. At present, three genera are acknowledged within the subfamily; however, their phylogenetic interrelations and systematic classification remain debated. In this study, the separation of Harpiola at the genus level was robustly supported by our phylogenomic analyses based on the mitochondrial genome, coding sequences (CDSs) and ultraconserved elements (UCEs) from 12 individuals covering all three genera of Murininae. Notably, a distinctive mito‐nuclear discordance emerged, with the nuclear genealogy ((Harpiocephalus, Harpiola), Murina) contrasting with the mitochondrial genealogy (Harpiocephalus, (Harpiola, Murina)). The integration of these findings with inferences of demographic history reveals that dramatic environmental changes during the Pleistocene glacial and inter‐glacial cycles have shaped the current distribution of Murininae. Moreover, the detection of extensive gene flow between ancient lineages of Harpiola and Murina suggests that an ancestral ‘ghost’ Murina lineage may have contributed its mitochondrial DNA, along with a limited portion of nuclear DNA, to Harpiola in a bygone hybridization zone. In addition to molecular analyses, we employed traditional and geometric morphometric analyses of skulls to differentiate the three genera. Harpiocephalus is readily distinguishable, but Harpiola and certain species of Murina exhibit overlapping characteristics both morphometrically and geometrically which may be the outcome of ancient introgression events. This finding highlights the importance of fine‐scale morphological distinctions within the latter genera, which may be the outcome of ancient introgression events.