The theoretical construct of an optimal offspring size remains widely cited in life history literature, despite the regular failure of the central prediction of that theory, that offspring size should not vary within populations. Here we used data from 77 litters collected over four years from captive and free-living northern water snakes (Nerodia sipedon) to test several hypotheses proposed to explain within-population variation in offspring size. Neonate mass varied from 1.5 to 6.1 g. Neonate mass did not increase as a simple function of maternal size, contrary to the hypothesis that maternal body size physically constrains offspring size. Holding litter size constant, larger females and females in better condition produced larger offspring. The variance in neonate size greatly exceeded the maximum that could be accounted for by the fractional-offspring hypothesis. We found some evidence that females that acquire food during the protracted period of follicular enlargement can invest that energy into those follicles, and thus increase offspring size. We found no evidence that embryos trade off condition with body size when they are born earlier. The strongest correlate of offspring size was litter size: offspring were smaller in larger litters. Because larger litters were born earlier, we propose that large females (i.e., those producing large litters) may have an energetic advantage that allows them to ovulate earlier. If early birth increases neonate fitness, then a small offspring born early may have the same fitness as a larger offspring born later, thereby allowing larger females to trade off offspring size against offspring number. Collectively, our results suggest that offspring size in northern water snakes varies as a consequence of constraints imposed by reproductive physiology, and potentially by adaptive maternal manipulation of offspring size. Understanding why offspring size varies is more likely to be advanced by an approach that incorporates both these types of factors, while discarding the construct of optimal offspring size.