Large variation in fish growth, even under controlled conditions, is not well understood. Size-based 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 competition on growth from those of other factors because it remains difficult to repeatedly measure the relevant physiological components contributing 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 modulator of both individual feed intake and costs of living inferred from growth. Using a Bayesian bioenergetic model, we estimated the mass-dependent scaling of intake and costs of living. Including relative size-effects on the allometric relationships for intake and costs of living improved model fit and explained 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.