There is strong evidence that genetic capacity for growth evolves toward an optimum rather than an absolute maximum. This implies that fast growth has a cost and that trade-offs occur between growth and other life-history traits, but the fundamental mechanisms are poorly understood. Previous work on the Atlantic silverside fish Menidia menidia has demonstrated a trade-off between growth and swimming performance. We hypothesize that the trade-off derives from the competing metabolic demands associated with growth and swimming activity. We tested this by measuring standard metabolic rate (M(STD)), maximum sustainable metabolic rate (M(ACT)) and metabolic scope of laboratory-reared silversides originating from two geographically distinct populations with well-documented differences in genetic capacity for growth. The fast-growth genotype had a significantly greater M(STD) than the slow-growth genotype, but a similar MACT when swum to near exhaustion. The scope for activity of the fast-growth genotype was lower than that of the slow-growth genotype. Furthermore, the fast-growth genotype eats larger meals, thereby incurring a greater postprandial oxygen demand. We conclude that a metabolic trade-off occurs between growth and other metabolic demands and that this trade-off provides a general mechanism underlying the evolution of growth rate.