The Kumamoto oyster Crassostrea sikamea is a marine bivalve naturally distributed along coasts of East Asia, with a hatchery population that has been under domestication in the US since its introduction from Japan in the 1940s. In the present research, we produced a chromosome-level genome assembly of C. sikamea and conducted whole genome resequencing of 141 individuals from the US hatchery population and 6 wild populations from China and Japan. The assembled C. sikamea genome was 616 Mb covering all 10 chromosomes with a contig N50 of 4.21 Mb and a scaffold N50 of 62.25 Mb. Synteny analysis revealed significant chromosomal rearrangements during bivalve evolution leading to oysters, but the 10 oyster chromosomes were well conserved over ~180 million years, indicating a disparity in bivalve chromosome evolution. Phylogenetic analysis produced three distinct clusters representing the US, Japanese and Chinese populations with the US population being closer to the Japanese population, conforming to origin of the former. The 402 genes that exhibited selection signals between the US and Japanese populations included 3 myosin heavy chain genes, which were also differentiated in domesticated lines of the eastern oyster, suggesting functional changes in muscle during domestication. Among the 768 genes that showed selection signals between the Japanese and Chinese populations, the most enriched included those involved in stress response, indicating the significance of stress defense in environmental adaptation. These findings have provided important insights into the evolution and environmental adaptation of bivalve, and generated useful resources for comparative genomics.