Bay scallop (Argopecten irradians) is an economically important bivalve species in China due to its fast growth rates and suitability for artificial breeding. There are five bay scallop subspecies distributed along the Atlantic coast of North America and the Gulf of Mexico that exhibit distinct growth and thermal stress tolerance characteristics, making them valuable resources for adaptive evolutionary studies. In this study, we used whole-genome resequencing analysis to uncover the genetic diversity and selective signatures of the bay scallop southern subspecies A. i. concentricus via comparison with the northern subspecies A. i. irradians. We identified a total of 15059961 high-quality single nucleotide polymorphisms (SNPs), of which 1616072 were unique to A. i. concentricus and 3319537 were unique to A. i. irradians. Following annotation analysis, a total of 23364701 effects were identified from the 15 million SNP sites. Only 2.819% of the loci were located in the exon regions; the majority of these SNPs were instead located in the intergenic (36.0%) and intron (32.3%) regions. Among the SNPs located within exons, silent mutations accounted for 55.1% (358166), missense mutations accounted for 43.7% (284415), and nonsense mutations accounted for 1.2% (7777). The total numbers of transitions and transversions across all SNPs were 97243196 and 82018037, respectively, resulting in a transitions/transversions ratio of 1.1856. Population structure, principal component analysis (PCA), and phylogenetic analysis based on genome-wide SNPs indicated significant genetic differentiation between A. i. concentricus and A. i. irradians. Linkage disequilibrium (LD) analysis showed that A. i. concentricus retained a higher level of LD compared to that of A. i. irradians, which may have been potentially influenced by domestication selection and inbreeding. Runs of homozygosity (ROH) analysis across the whole genome revealed that A. i. concentricus retained more ROH, indicating a higher level of inbreeding. Population genetic diversity analysis revealed a decrease in genetic diversity in certain regions of the A. i. concentricus genome compared to those of the northern subspecies population; this may be the result of continuous artificial selection for heat tolerance and inbreeding. Selective sweep analysis of A. i. irradians revealed 349 genes under positive selection, including GHSR, HSF1, HABP2, and DnaJ, which may be related to its corresponding rapid growth rate, strong heat tolerance, high immunity, and other environmental adaptation characteristics. Functional enrichment analysis revealed that the genes located in the selective sweep regions were primarily associated with cell signal transduction, maintenance of cell morphology, and regulation of metabolic processes. Overall, this study sheds light on the genetic differentiation and signatures of selection in bay scallop subspecies, thereby providing a valuable resource for scallop genomic research and molecular breeding.