Predicting the potential for species adaption to climate change is challenged by the need to identify the physiological mechanisms that underpin species vulnerability. Here, we investigated the sensitivity to ocean acidification in marine mussels during early development, and specifically the trochophore stage. Using RNA and DNA sequencing and in situ RNA hybridization, we identified developmental processes associated with abnormal development and rapid adaptation to low pH. Trochophores exposed to low pH seawater exhibited 43 differentially expressed genes. Gene annotation and in situ hybridization of differentially expressed genes point to pH sensitivity of (1) shell field development and (2) cellular stress response. Five genes within these two processes exhibited shifts in allele frequencies indicative of a potential for rapid adaptation. This case study contributes direct evidence that protecting species’ existing genetic diversity is a critical management action to facilitate species resilience to climate change.