The impact of ocean acidification on marine invertebrate eggs and consequences for sperm chemotaxis are unknown. In the sea urchins Heliocidaris tuberculata and H. erythrogramma, with small (93µm) and large (393µm) eggs, respectively, we documented the effect of decreased pH on the egg jelly coat, an extracellular matrix that increases target size for sperm and contains sperm attracting molecules. In near future conditions (pH 7.8, 7.6) the jelly coat of H. tuberculata decreased by 11 and 21%, reducing egg target size by 9 and 17%, respectively. In contrast, the egg jelly coat of H. erythrogramma was not affected. The reduction in the jelly coat has implications for sperm chemotaxis in H. tuberculata. In the presence of decreased pH and egg chemicals, the sperm of this species increased their velocity, motility and linearity, behaviour that was opposite to that seen for sperm exposed to egg chemicals in ambient conditions. Egg chemistry appears to cause a reduction in sperm velocity where attractants guide them in the direction of the egg. Investigation of the effects of decreased pH on sperm isolated from egg chemistry does not provide an integrative assessment of the effects of ocean acidification on sperm function. Differences in the sensitivity of the jelly coat of the two species is likely associated with egg evolution in H. erythrogramma. We highlight important unappreciated impacts of ocean acidification on marine gamete functionality, and insights into potential winners and losers in a changing ocean, pointing to the advantage conveyed by evolution of large eggs.