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 M_ACT 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.