Combining population genetics with genomic data has transformed scientist’s ability and resolution of making ecological inferences, thus making it possible to detect previously unidentified structures and obtain more accurate estimates of demographic parameters in wild populations. Ark shell is an economically and ecologically important marine species for fisheries industry in China, but its habitats have been severely damaged due to overexploitation of natural resources. Recently, protection of the ark shell as a natural resource has attracted extensive attention. Here, we identified 10,108 single-nucleotide polymorphisms using Restriction-site Associated DNA Sequencing (2b-RAD) to explore the structure of seven populations of S. broughtonii from the Asian Pacific Northwest region (four sites in China, two in Korea, and one in North Korea). A high level of genetic diversity was detected in all seven S. broughtonii populations. Pairwise FST estimates and neighbor-joining (NJ) tree topologies showed a clear division between the populations from China and Korea, and Chinese populations exhibited low levels of divergence from one another. This significant genetic divergence of the Chinese population implies that translocation of individuals for aquaculture should be properly managed for the preservation of genetic diversity and eventual local adaptation in natural populations.