Natural genetic variation is a valuable source of resilience to changing environments. The eastern oyster (Crassostrea virginica) lives in spatio-temporally highly variable environments. This species is able to survive in a wide variety of environments due to its physiological plasticity, evolutionary adaptation to specific environments, or both. It is well-recognized that the evolution of resilience to climate related stressors depends on the standing stock of genetic variation. This study aimed at the identification of molecular pathways associated with oyster resilience to ocean acidification (OA). Adult oysters were spawned and larvae were reared in ambient (pCO₂ of ~600 ppm) or acidified (~1200 ppm) conditions immediately upon fertilization. RNA and DNA samples were collected before larvae were moved to pCO₂ treatments, after 96 hours in treatments, and after metamorphosis. Samples were processed for gene expression using RNASeq and SNP profiling by ddRADSeq. Detected variants from survivors of OA were related to biomineralization, calcium ion binding, cell differentiation, ion channel activity and hemocyte function. Upregulated genes under OA conditions included genes related to the above functions as well as response to stress. Downregulated genes were involved in immunity and cell signaling. Overall, metamorphosis appeared to be more of a selective pressure than larval development. This research indicates that resilience to OA is at least partially dictated by genetics.