Given current anthropogenic alterations to many ecosystems and communities, it is becoming increasingly important to consider whether and how organisms can cope with changing resources. Metabolic rate, because it represents the rate of energy expenditure, may play a key role in mediating the link between resource conditions and performance and thereby how well organisms can persist in the face of environmental change. Here, we focus on the role that energy metabolism plays in determining organismal responses to changes in food availability over both short-term ecological and longer-term evolutionary timescales. Using a meta-analytical approach encompassing multiple species, we find that individuals with a higher metabolic rate grow faster under high food levels but slower once food levels decline, suggesting that the association between metabolism and life-history traits shifts along resource gradients. We also find that organisms can cope with changing resource availability through both phenotypic plasticity and genetically based evolutionary adaptation in their rates of energy metabolism. However, the metabolic rates of individuals within a population and of species within a lineage do not all respond in the same manner to changes in food availability. This diversity of responses suggests that there are benefits but also costs to changes in metabolic rate. It also underscores the need to examine not just the energy budgets of organisms within the context of metabolic rate but also how energy metabolism changes alongside other physiological and behavioural traits in variable environments.