Juveniles must reach a critical body size to become a mature adult. Molecular determinants of critical size have been studied, but the evolutionary importance of critical size is still unclear. Here, using nine fly species, we show that interspecific variation in organism size can be explained solely by species-specific critical size. The observed variation in critical size quantitatively agrees with the interspecific scaling relationship predicted by the life history model, which hypothesizes that critical size mediates an energy allocation switch between juvenile and adult tissues. The mechanism underlying critical size scaling is explained by an inverse relationship between growth duration and growth rate, which cancels out their contributions to the final size. Finally, we show that evolutionary changes in growth duration can be traced back to the scaling of ecdysteroid hormone dynamics. We conclude that critical size adaptively optimizes energy allocation, and has a central role in organism size determination.