Studying the adaptive divergence of shellfish inhabiting different environments is crucial to predict the resilience of marine organisms to rapid climate change. Although the shell serves as the primary physical barrier against environmental change, the evolutionary adaptation of biomineralization in shellfish remains poorly understood. In this study, we using common garden designs to investigate the shell matrix proteome of estuarine (Crassostrea ariakensis) and Pacific (Crassostrea gigas) oysters inhabiting estuarine and open coastal zones, respectively. Shell matrix proteome analyses revealed extensive domain expansion of classical pathway secretomes, which likely contribute to the enhanced biomineralization capacity of estuarine oysters. Furthermore, two-thirds of the 27 C. ariakensis-specific shell matrix-secreted proteins (SMSPs) lacked homology with known proteins in the Swiss-Prot and nr databases, indicating rapid evolution. Our findings suggest that intensified classical pathway secretomes and rapid evolution of species-specific SMSPs are key factors shaping the defense of shells to enhance their adaptive potential to climate change.