Drivers of large variation in observed fish growth, even under controlled conditions such as in aquaculture experiments, are not well understood. Size-based intraspecific competition is known to influence processes which lead to variation in both intake and growth. Yet, it is challenging to tease apart the effects of competitive interactions on fish growth from those of other factors because it remains difficult to repeatedly measure the relevant components of individual fish physiology that contribute to growth. We used an extensive longitudinal dataset of individual-level intake and growth measurements of 543 fish sampled from an aquaculture experiment to test the effects of relative body size as a proxy for competitive ability. This, in turn, was investigated as potential modulator of both individual feed intake and costs of living inferred from growth in a bioenergetic model. Using a Bayesian approach to integrate data and model, we estimated the mass-dependent scaling of intake and costs of living. Including relative size-effects on the allometric relationships for both intake and costs of living improved model fit and allowed us to reproduce a large part of the observed size variation. This implies that size-dependent competitive interactions are an important driver of size-at-age variation. Our results also indicate that growth depression in smaller than average fish is more significantly impacted by size-based competition effects on costs of living rather than on feed intake.