Reproduction includes two energy investments-the energy in the offspring and the energy expended to make them. The former is well understood, whereas the latter is unquantified but often assumed to be small. Without understanding both investments, the true energy costs of reproduction are unknown. We present a framework for estimating the total energy costs of reproduction by combining data on the energy content of offspring (direct costs) and the metabolic load of bearing them (indirect costs). We find that direct costs typically represent the smaller fraction of the energy expended on reproduction. Mammals pay the highest reproductive costs (excluding lactation), ~90% of which are indirect. Ectotherms expend less on reproduction overall, and live-bearing ectotherms pay higher indirect costs compared with egg-layers. We show that the energy demands of reproduction exceed standard assumptions.