Marine invertebrates, such as oysters, were once thought to form large, panmictic populations with little genetic differentiation due to their high reproductive capacity and dual life stages. However, recent studies have shown significant genetic structuring and moderate gene flow across populations, influenced by factors like ocean currents, historical climate events, and environmental changes. The black-lip oyster (Saccostrea echinata), with its extensive dispersal potential, is ideal for population genetics studies. In current study, mitochondrial DNA (COI gene) was utilized to investigate the population structure, genetic diversity, and demographic history of S. echinata in the northern South China Sea (NSCS) and Beibu Gulf. Results revealed high genetic diversity with 82 haplotypes from 190 specimens, a star-shaped haplotype network, and significant genetic differentiation, with most variation occurring within populations. Genetic analysis identified three distinct genetic groups across the sampled regions. Historical demographic analysis indicated population expansion approximately 44–155 Kya after the Last Glacial Maximum. Genetic structure was shaped by historical climatic events causing isolation and secondary contact, as well as contemporary ocean currents influencing gene flow. The study highlights the complex interplay of genetic diversity, population structure, and historical dynamics in S. echinata, with implications for conservation and aquaculture in the Asia-Pacific region.