Significance The pH of the global ocean is decreasing due to the absorption of anthropogenically emitted CO ₂ , causing ocean acidification (OA). OA negatively impacts marine shellfish and threatens the continuing economic viability of molluscan shellfish aquaculture, a global industry valued at more than 19 billion USD. We identify traits linked to growth and lipid regulation that contribute tolerance to OA in abalone aquaculture, with broader implications for adaptation efforts in other shellfish species. We also identify evolved heritable variation for physiological resilience to OA that may be exploited in commercial and restoration aquaculture breeding programs to offset the negative consequences of continuing climate change.