The presumption is that egg quality influences larval survival and that egg size influences egg quality. Thus, larger eggs should be favored by selection. Counterweighing the tendency for egg size to increase is the number of eggs that can be produced if egg size remains small. We examine how egg size and egg number counterbalance in Crassostrea oysters, resulting in an average egg size near 50 µm. Simulations imposing a diversity of ranges in larval survivorship—from little advantage for large eggs relative to small eggs to a great advantage—yield some anticipated outcomes in which genotypes generating larger eggs are favored. In other simulations, however, genotypes generating smaller eggs became increasingly common. In these cases, egg size declines, as does the likelihood of survival of individual larvae: the antithesis of expectation. Few simulations identify preferred egg sizes near the size typically observed, suggesting that, under most field conditions, a selective advantage exists for smaller or larger eggs than those typically spawned. However, the extremes in egg size are rarely advantageous. Most simulations resolve an optimal intermediate egg size. Thus, observed egg size is a balance between the chanciness of larval survival enhanced by the production of a larger number of eggs and the genetically predisposed, but environmentally modulated, individual probability of larval survival that is a function of egg size, with environment determining the optimal size. The 50-µm size observed likely represents the median outcome of a range of larval survivorship probabilities, each selecting for relatively larger or smaller eggs, imposed stochastically over multiple generations. In this scenario, each year the population is pulled toward smaller or larger egg sizes, but in the next year the impetus is independent of the previous year. Reduced generation time, by disease or fishing, modifies the extent, but not the direction of trend. Thus, environmental stochasticity retains preeminence in stabilizing a balance between the probabilities of survival modulated by egg number and by egg size. The influence of shortened generation time—by disease, for example—is unlikely to be manifest in a modification in egg size and hence egg number.