Hong Kong oyster Crassostrea hongkongensis is an important aquaculture species in the coastal areas of southern China. Because of its high demand and reasonable price, the production of Cohnella hongkongensis has increased drastically. However, the aquaculture of C. hongkongensis has also encountered some problems, such as seasonal mass mortality and reduction of availability and quality of wild seeds. Genetic linkage map is an effective tool for analyzing economically important traits. In this study, a consensus genetic map of C. hongkongensis was constructed by using microsatellite markers of F1 family. The consensus linkage map contained 104 loci, with a span of 653.9 cM and an average resolution of 6.9 cM. The estimated coverage of consensus linkage map was 85%. We identified 10 linkage groups, which were consistent with the haploid chromosome number of the species. The linkage map of male C. hongkongensis comprised 57 markers with a span of 467.6 cM, while the linkage map of female C. hongkongensis comprised 72 markers with a span of 570.9 cM. The average recombination ratio between males and females was 1:1.2. This map is vital for future QTL mapping framework of C. hongkongensis to perform marker assisted selection. Moreover, compared with di-nucleotide microsatellite markers, tri-nucleotide microsatellite markers have significantly stronger correlation with functional genes and cross-amplification success. We also found that the application potential of tri-nucleotide microsatellite markers in molecular-marker assisted selection gene mapping, and comparative linkage mapping was greater than that of di-nucleotide markers. •The first genetic linkage map for Crassostrea hongkongensis exclusively using microsatellite markers.•The consensus linkage map contained 10 linkage groups, which comprised 104 loci.•Females tend to have higher recombination rate than males.•The tri-nucleotide microsatellite markers have a higher correlation with functional genes than di-nucleotide markers.