Some marine ecosystems already experience natural declines in pH approximating those predicted with future anthropogenic ocean acidification (OA), the decline in seawater pH caused by the absorption of atmospheric CO2. The molecular mechanisms that allow organisms to inhabit these low pH environments, particularly those building calcium carbonate skeletons, are unknown. Also uncertain is whether an enhanced capacity to cope with present day pH variation will confer resistance to future OA. To address these issues, we monitored natural pH dynamics within an intertidal habitat in the Northeast Pacific, demonstrating that upwelling exposes resident species to pH regimes not predicted to occur elsewhere until 2100. Next, we cultured the progeny of adult purple sea urchins (Strongylocentrotus purpuratus) collected from this region in CO2-acidified seawater representing present day and near future ocean scenarios and monitored gene expression using transcriptomics. We hypothesized that persistent exposure to upwelling during evolutionary history will have selected for increased pH tolerance in this population and that their transcriptomic response to low pH seawater would provide insight into mechanisms underlying pH tolerance in a calcifying species. Resulting expression patterns revealed two important trends. Firstly, S. purpuratus larvae may alter the bioavailability of calcium and adjust skeletogenic pathways to sustain calcification in a low pH ocean. Secondly, larvae use different strategies for coping with different magnitudes of pH stress: initiating a robust transcriptional response to present day pH regimes but a muted response to near future conditions. Thus, an enhanced capacity to cope with present day pH variation may not translate into success in future oceans.