Metabolic scaling with allometric exponents (0.66 < b < 1) is a well-recognized phenomenon across all living systems and providing the cornerstone for the metabolic theory of ecology. Metabolic scaling relationships connect individual physiology to broad scale ecology, and are incorporated in multi-scale bioenergetics research to support academic and applied science. Whether the scaling exponent is universal is hotly debated as many continue to identify variation in metabolic scaling relationships. Contextual sources of variation include, taxonomic groups, ecological roles and lifestyles, and environmental conditions. Individual activity level (active vs resting state) also changes metabolic scaling: active metabolic rates (AMR) are predicted to scale with exponents b_AMR ~ 1, and resting metabolic rates (RMR) with b_RMR < 1. However, it is largely unknown how AMR scales across different contexts, and how b_AMR and b_RMR relate within these contexts. We explored and compared the variation in scaling of AMR and RMR in fishes with different body shapes and ecologies. Contrary to predictions, we found lower scaling exponent for AMR than RMR (b_AMR < b_RMR) in fish taxa. Further, we found different scaling relationships of AMR and RMR for demersal and reef-associated fish, short-deep and fusiform shaped fish, temperate and tropical fish, salt and freshwater fish. And we found no evidence for consistent relationships between context-specific scaling of RMR and AMR (all associations were observed: b_AMR > b_RMR, b_AMR < b_RMR, b_AMR ~ b_RMR). As signified by our results, it is important to consider both, the metabolic state (active and resisting) and life-history characteristics, to ensure robust inference about changing metabolism-dependent biological processes.