The subgenusCerasus(Rosaceae) contain numerous fruit trees and ornamentals with high economic values. The origin and genetic divergence among various types of fruiting cherries always remain a perplexing issue. We employed three plastom fragments and ITS sequence matrices derived from 912 cherry accessions to elucidate the phylogeographic structure and genetic relationship among fruiting cherries, as well as the origin and domestication of cultivated Chinese cherry. The integration of haplotype genealogies, Approximate Bayesian computation (ABC) approach and estimation of genetic differentiation within and between different groups and lineages has facilitated the resolution of several previously unresolved questions. Firstly, distant phylogenetic relationships betweenCerasusandMicrocerasusaccessions, as indicated by both nuclear and chloroplast data, suggested independent origins and evolution for these two taxa. Moreover, two distinct geographic origin centers (Europe and China) have been confirmed, with significant phylogeographic signals and high genetic differentiation observed between cherries from these regions. This may be attributed to long-term geographic isolation caused by Himalaya-Hengduan Mountains. Our phylogeographic analyses and ABC analysis suggested that cherries inhabiting in China may have undergone multiple hybridization events during the glacial refugia of the eastern edge and southern Himalaya-Hengduan Mountains, followed by rapid radiation throughout their current habitats during interglacial period. The discrepancy between nuclear and chloroplast data may be attributed to hybridization events and incomplete lineage sorting. Furthermore, we speculated that the domesticated Chinese cherries were derived from wild accessions in Longmenshan Fault Zones approximately 2600 years ago. We have also traced the domestication processes and dispersal routes of cultivated Chinese cherries.