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Abstract The theory describing the evolution of offspring size often assumes that the production cost per unit volume is the same for small and large offspring. However, this may not be true if indirect costs of reproduction (e.g., material and energetic costs of supporting offspring development) scale disproportionately with offspring size. Here we show how direct and indirect costs of reproduction can be explicitly modeled within the Smith–Fretwell framework and how observations of size-number relationships can thus be used to evaluate indirect costs. We applied this analysis to measures of egg volume and fecundity for over 300 individuals of a coastal fish species and found that the tradeoff was much stronger than the expected inverse (fecundity scaled with volume−1.843). Larger offspring were thus more expensive to produce. For our study species, an important indirect cost was that larger eggs were accompanied by disproportionately more ovarian fluid. Calorimetry and removal experiments were used to further measure both the energetic costs and fitness benefits of ovarian fluid. In addition, we show that indirect costs of reproduction can intensify size-number tradeoffs in a variety of fishes. Indirect costs of reproduction can be large and may therefore play an important role in the evolution of offspring size.