The allocation of metabolic energy to growth fundamentally influences all levels of biological organisation. Here we use a first‐principles theoretical model to characterise the energetics of fish growth at distinct ontogenetic stages and in distinct thermal regimes. Empirically, we show that the mass scaling of growth rates follows that of metabolic rate, and is somewhat steeper at earlier ontogenetic stages. We also demonstrate that the cost of growth, $E_m$, varies substantially among fishes, and that it may increase with temperature, trophic level and level of activity. Theoretically, we show that $E_m$ is a primary determinant of the efficiency of energy transfer across trophic levels, and that energy is transferred more efficiently between trophic levels if the prey are young and sedentary. Overall, our study demonstrates the importance of characterising the energetics of individual growth in order to understand constraints on the structure of food webs and ecosystems.