How steeply metabolic rate and growth rate change (scale) with body mass, and their causal relationship, has been hotly debated for over a century. Prevailing theory argues that metabolic and growth rates are physically constrained to scale in the same way for all organisms, with body mass0.75. Rivalling life-history optimisation theory suggests that scaling can vary and is shaped by evolutionary optimisation of energy allocation among metabolic rate, growth, and reproduction. However, past research has almost exclusively investigated metabolic scaling across individuals or species, not within individuals as they grow through ontogeny. This is critical oversight, as body mass is gained through growth, and bodily growth occurs within individuals. Here, we longitudinally measured body mass and both standard (maintenance) and maximum metabolic rates (and thus metabolic scope) on average 6.6 times within the same 389 individuals from seven fish species. We uncover previously unrecognized co-variation in the within-individual (ontogenetic) scaling of metabolic and growth rates: scaling of standard metabolic rate correlates positively with scaling of growth rate, while scaling of metabolic scope corelates negatively with scaling of growth rate. This indicates a trade-off whereby accelerating ontogenetic growth comes at a cost of reduced metabolic scope to support functions beyond maintenance. Our results challenge traditional 0.75-power scaling and new life-history optimisation theory that predicts a negative correlation between ontogenetic scaling of metabolic rate and growth. Our findings also suggest that unaccounted variation in growth is a likely explanation for the century-long debate about whether, and to what extent, metabolic scaling varies.