Hyperallometric reproduction, whereby large females contribute relatively more to the renewal of the population than small females, is purported to be widespread in wild populations, especially in fish species. Bioenergetic models derived from a sufficiently general metabolic theory should be able to capture such a relationship but it was recently stated that no existing models adequately capture hyperallometric reproduction. If this were true it would seriously challenge our capacity to develop robust predictions of the life history and population dynamics in changing environments for many species. Here, using the European sea bass (Dicentrarchus labrax) as a test case, we demonstrate multiple ways that hyperallometric reproduction in a population may emerge from the Dynamic Energy Budget (DEB) theory, some inherently related to the metabolism and life history and others related to plastic or genetically based intraspecific variation. In addition, we demonstrate an empirical and modelled hypoallometric scaling of reproduction in this species when environment is controlled. This work shows how complex metabolic responses may underlie apparently simple relationships between weight and reproduction in the wild and provides new and testable hypotheses regarding the factors driving reproductive scaling relationships found in the wild.