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Cherries (subg. Cerasus) belong to Prunus s.l. (Rosaceae) and are widely distributed in temperate and subtropical regions of the Northern Hemisphere. Given its ornamental and edible functions, it is a hugely preferred germplasm resource for human societies. However, the interspecific phylogenetic relationships, divergence times, and routes of this subgenus remain unclear. To reveal its enigmatic and intricate evolutionary history, we newly sequenced 12 subg. Cerasus species, reconstructed the plastome phylogeny with 24 previously published subg. Cerasus species. This study supports that subg. Cerasus split into five clades, among which P. mahaleb is the basal group of subg. Cerasus ; P. campanulata is genetically distantly related to P. cerasoides and is not recommended for treatment as a variety of the latter; P. subhirtella is involved in the speciation of P. yedoensis. Molecular dating and ancestral area reconstructions infer that subg. Cerasus originated in the Eastern Mediterranean–Central Asia before 11.57 Mya (95% HPD = 5.34–19.1 Mya) and subsequently spread into the Qinghai-Tibetan Plateau (QTP) and adjacent regions. The first dispersal event of modern subg. Cerasus was facilitated by 'out-of-QTP', colonizing North America across the Bering Land Bridge and re-dispersing into Europe from the Late Miocene to Pliocene and forming the initial distribution pattern of extant subg. Cerasus in the Pliocene; The end of the Quaternary glacial period witnessed a second dispersal event, and core subg. Cerasus population diversity flourished radially in its separate refugia during the Late Pleistocene. [ABSTRACT FROM AUTHOR]