Rising levels of atmospheric CO2 are altering global ocean chemistry, including a decline in the pH of surface waters. Under more acidified conditions, marine organisms that build shells and skeletons are under increasing risk of a reduction in their ability to deposit calcium carbonate. Relatively little is known about genetic variation in the capacity of organisms to respond to such effects. We examined skeletal growth in larval sea urchins to examine genetic variation in their sensitivity to elevated CO2 under exposure at two life history stages: at fertilization, and during larval development. Using gametes of the purple-spined sea urchin (Arbacia puncutlata), we carried out single-pair crosses in blocks of 3 males x 3 females for a total of 9 sibships, repeated over 7 blocks. Fertilizations were done in seawater saturated at either current (392 ppm) or 2.5x-current (980 ppm) CO2, and the resulting embryos from each cross were reared over 3 days to four-arm larvae under each of the same two CO2 conditions. Nine landmarks on larvae were used to calculate both skeletal and soft body measurements. Exposure to elevated CO2 during larval development significantly reduced the length of the postoral arms and body rods and increased postoral arm asymmetry. Surprisingly, exposure to elevated CO2 during fertilization also reduced the subsequent growth of anterolateral arms, body rods, and body length. We found significant additive and non-additive genetic variation for growth of certain characters but no evidence of genetic variation for the effects of elevated CO2 on growth. These results suggest that this population may not have the genetic capacity for an evolutionary response to elevated CO2 under predicted near-future conditions.