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Cherries (<i>Prunus</i> Subgenus <i>Cerasus</i>) have economic value and ecological significance, yet their phylogeny, geographic origin, timing, and dispersal patterns remain challenging to understand. To fill this gap, we conducted a comprehensive analysis of the complete chloroplast genomes of 54 subg. <i>Cerasus</i> individuals, along with 36 additional genomes from the NCBI database, resulting in a total of 90 genomes for comparative analysis. The chloroplast genomes of subg. <i>Cerasus</i> exhibited varying sizes and consisted of 129 genes, including protein-coding, transfer RNA, and ribosomIal RNA genes. Genomic variation was investigated through InDels and SNPs, showcasing distribution patterns and impact levels. A comparative analysis of chloroplast genome boundaries highlighted variations in inverted repeat (IR) regions among <i>Cerasus</i> and other <i>Prunus</i> species. Phylogeny based on whole-chloroplast genome sequences supported the division of <i>Prunus</i> into three subgenera, I subg. <i>Padus</i>, II subg. <i>Prunus</i> and III subg. <i>Cerasus</i>. The subg. <i>Cerasus</i> was subdivided into seven lineages (IIIa to IIIg), which matched roughly to taxonomic sections. The subg. <i>Padus</i> first diverged 51.42 Mya, followed by the separation of subg. <i>Cerasus</i> from subg. <i>Prunus</i> 39.27 Mya. The subg. <i>Cerasus</i> started diversification at 15.01 Mya, coinciding with geological and climatic changes, including the uplift of the Qinghai–Tibet Plateau and global cooling. The Himalayans were the refuge of cherries, from which a few species reached Europe through westward migration and another species reached North America through northeastward migration. The mainstage of cherry evolution was on the Qing–Tibet Plateau and later East China and Japan as well. These findings strengthen our understanding of the evolution of cherry and provide valuable insights into the conservation and sustainable utilization of cherry’s genetic resources.