Abstract: Babylonia areolata is an essential marine economic mollusk found in the shallow seas of tropical and subtropical regions. In mainland China, native species such as B. areolata and B. lutosa have developed into a large-scale aquaculture industry, making China the largest culture producer worldwide. However, basic biological research on B. areolata was still very rare, which constrains the improvement of aquaculture techniques. We successfully constructed a chromosome-level genome containing 35 chromosomes, with a total genome length of approximately 1.65 Gb and scaffold and contig N50 lengths of 53.17 Mb and 2.64 Mb, respectively. Compared with the genomes of several Neogastropoda species currently available, the reference genomes reached the highest assembly and annotation levels. Using whole-genome resequencing data from 113 wild specimens collected from five geographical populations, the study found that these samples could be divided into three main genetic groups: Thailand, Vietnam, and China. For the first time, this study determined that the sex determination system of the B. areolata is a female heterogametic ZZ/ZW type. A sex-specific molecular marker based on an 81 bp female-specific deletion was successfully developed and validated across different geographical populations. These findings enhance our understanding of the genetic mechanisms in the B. areolata and provide a solid scientific foundation for molecular breeding and genetic improvement.