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The clam Coelomactra antiquata (Spengler, 1802) is one of the most economically important marine bivalves in China. Previous genetic analysis shows that C. antiquata possibly consists of two cryptic species, a northern and a southern lineage. Some differences between the two lineages are observed in their morphology and fitness in aquaculture. However, little is known about the genetic basis of these differences. In this study, a comparative transcriptomics study was performed to provide additional information for delineating the cryptic species of C. antiquata, as well as insights into the adaptive evolution in the southern lineage of C. antiquata. A total of 4377 orthologous genes were identified using a phylogenetic tree-based approach. The Kimura 2-parameter genetic distances were 0.0385 between the two lineages of C. antiquata, and 0.006 within the northern lineage. The sequence divergences supports that the lineages represent two cryptic species. We identified 28 positively selected genes (PSGs) from the southern lineage of C. antiquata using a modified branch-site model. The PSGs were implicated in innate immune responses, metabolism, development, cell division, transmembrane transport, and signaling processes, which could be related to the higher disease resistance, growth rate, and adaptability of the southern lineage than its northern counterpart. The comparative transcriptome analysis provides a foundation for future investigations on the biological differences between the two lineages of C. antiquata.