Various models that assume correlations between maternal phenotype and offspring environment predict adaptive variation in egg size within populations. Here we conduct a comparative test of these models using published data on fish egg size. Intrapopulation variation in egg size was most pronounced in fish with demersal eggs and larvae (median coefficient of variation [CV] at family level = 6.5%), where offspring environment is likely influenced by maternal phenotype, and least so in fish with pelagic eggs (CV = 3.6%), which experience a relatively stochastic spatial distribution during incubation. This difference was significant at various taxonomic levels, was robust to variation in mean egg size and habitat (i.e., freshwater or marine), and was mirrored in independent paired contrasts. Fish with demersal eggs and pelagic larvae were not significantly different from those with pelagic eggs (CV = 3.8%), indicating that selection favoring within-population variation in egg size occurs mainly posthatching and that any such selection occurring prehatching may be less intense. These results suggest that patterns of within-population variation in egg size among fish taxa reflect adaptive processes and that maternal effects on the egg size-fitness function may explain apparent discrepancies from the single-optima Smith-Fretwell model.