Cerasus is a subgenus of Prunus in the family Rosaceae that is popular owing to its ornamental, edible, and medicinal properties. Understanding the evolution of the Cerasus subgenus and identifying selective trait loci in edible cherries are crucial for the improvement of cherry cultivars to meet producer and consumer demands. In this study, we performed a de novo assembly of a chromosome-scale genome for the sweet cherry (Prunus avium L.) cultivar 'Burlat', covering 297.55 Mb and consisting of eight chromosomes with 33,756 protein-coding genes. The resequencing and population structural analysis of 384 Cerasus representative accessions revealed that they could be divided into four groups (Group 1, Group 2, Group 3, and Group 4). We inferred that Group 1 was the oldest population and Groups 2, 3, and 4 were clades derived from it. In addition, we found selective sweeps for fruit flavor and improved stress resistance in different varieties of edible cherries (P. avium, P. cerasus, and P. pseudocerasus). Transcriptome analysis revealed significant differential expression of genes associated with key pathways, such as sucrose starch and sucrose metabolism, fructose and mannose metabolism, and the pentose phosphate pathway, between the leaves and fruits of P. avium. This study enhances the understanding of the evolutionary processes of the Cerasus subgenus and provides resources for functional genomics research and the improvement of edible cherries.