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Although recent molecular phylogenetic analyses have greatly improved our understanding of the classification of the large liverwort family Lejeuneaceae, the frequent incongruencies between morphology‐based taxonomy and molecular phylogeny have hindered our understanding of evolutionary diversification within the group. Here we focus on Leptolejeunea (Spruce) Steph., a pantropical epiphyllous genus in Lejeuneaceae with 40 species. Phylogenetic studies on the genus have been hampered by insufficient taxon sampling, leaving the deep phylogenetic relationships within this group unresolved. We present the most comprehensive phylogenetic analysis of the genus to date with sampling of over 80% of species, including the enigmatic Leptolejeunea spinistipula (Mizut.) X.L.He endemic to Borneo. Based on data from three molecular markers with representatives of Leptolejeunea and its allies, Leptolejeunea appeared to be monophyletic following the exclusion of L. spinistipula and its transfer to Soella R.L.Zhu, L.Shu, Qiong He & Y.M.Wei. A total‐evidence approach was taken to resolve the backbone phylogeny of Leptolejeunea and a first infrageneric classification of Leptolejeunea, including a new subgenus and three new sections, is proposed based on integrated molecular and morphological evidence. Reconstruction of the evolutionary history showed a wide ancestral area of Leptolejeunea during the Paleogene that arose in mainland Asia, followed by an accelerated speciation rate. Across the biogeographical history of Leptolejeunea, long‐distance dispersal had profound effects on population expansion. Our findings suggest that Australasia is a source of biodiversity of Asian evergreen broad‐leaved forests that have been established since the Oligocene and rose after the early Miocene. [ABSTRACT FROM AUTHOR]