Hawthorns (Crataegus L.) are widely distributed and well known for their medicinal properties and health benefits. Nevertheless, the phylogenetic relationships among Crataegus native to China remain unclear. Additionally, no consensus exists on the origin and evolution of Crataegus, and the relationship between Crataegus and Mespilus is is unclear. Here, we sequenced 20 chloroplast (cp) genomes (19 from Crataegus and 1 from Mespilus) and combined them with 2 existing cp genomes to investigate the phylogenetic relationships, divergence times and biogeographic history of Crataegus. Four hypervariable loci emerged from the newly sequenced genomes. The phylogenetic results indicated that the 14 Chinese Crataegus species analyzed clustered into two clades. One clade and the North American Crataegus species grouped together, while the other clade grouped with the European Crataegus species. Our results favor recognizing Mespilus and Crataegus as one genus. Molecular dating and biogeographic analyses showed that Crataegus originated in Southwest China during the early Oligocene, approximately 30.23 Ma ago. Transoceanic migration of East Asian Crataegus species across the Bering land bridge led to the development of North American species, whereas westward migration of the ancestors of C. songarica drove the formation of European species. C. cuneata may represent the earliest lineage of Chinese Crataegus. The uplift of the Qinghai–Tibet Plateau (QTP) and the Asian monsoon system may have led the ancestors of C. cuneata in south-western China to migrate toward the northeast, giving rise to other Chinese Crataegus species. This study offers crucial insights into the origins of Crataegus and proposes an evolutionary model for the genus.