Cupped oysters (Ostreidae, genus Crassostrea) occupy nearshore marine and estuarine habitats worldwide, providing many ecosystem goods and services as well as being a commercially important group of bivalves. In this study, the species identification of an “adulterant” oyster with small body size, which is often misidentified as a “young individual” of other sympatric species, including C. sikamea and C. hongkongensis, was determined for the first time, based on molecular markers (partial mitochondrial cox1 and rrnL genes), phylogenetic analysis, and morphometric approaches. This novel species, C. zhanjiangensis, commonly known as the “cat ear oyster” in Guandu (a famous estuarine oyster farming region of Zhanjiang, Guangdong Province, China), appears to potentially influence the efficiency of C. hongkongensis spat collection due to niche competition on spat collection devices. Phylogenetic analyses confirm its status as the most basal taxon of the Indo-Pacific Crassostrea. A comparative study of the shell characteristics of C. zhanjiangensis, and other Crassostrea species revealed several distinctive morphological traits, including a generally smaller body size, a deeply cupped left valve, and a right valve that is convex in adults but flat in young individuals. Other distinctive features of the new species include life cycle traits that are unique compared with the sympatric C. hongkongensis and C. sikamea species, such as a higher growth rate in the fast growth phase after settlement, followed by a significantly slower growth rate and mass mortality during subsequent life stages. This study provides the basic information necessary for further ecological and population genetic studies on this new species.