According to the metabolic theory of ecology, metabolic rate, an important indicator of the pace of life, varies with body mass and temperature due to internal physical constraints. However, various ecological factors may also affect metabolic rate and its scaling with body mass. Although reports of such effects on metabolic scaling usually focus on single factors, the possibility of significant interactive effects between multiple factors requires further study. In this study, we show that the effect of temperature on the ontogenetic scaling of resting metabolic rate of the freshwater amphipod Gammarus minus depends critically on habitat differences in predation regime. Increasing temperature tends to cause decreases in the metabolic scaling exponent (slope) in population samples from springs with fish predators, but increases in population samples from springs without fish. Accordingly, the temperature sensitivity of metabolic rate is not only size-specific, but also its relationship to body size shifts dramatically in response to fish predators. We hypothesize that the dampened effect of temperature on the metabolic rate of large adults in springs with fish, and of small juveniles in springs without fish are adaptive evolutionary responses to differences in the relative mortality risk of adults and juveniles in springs with versus without fish predators. Our results demonstrate a complex interaction among metabolic rate, body size, temperature, and predation regime. The intraspecific scaling of metabolic rate with body size and temperature is not merely the result of physical constraints related to internal body design and biochemical kinetics, but rather is ecologically sensitive and evolutionarily malleable.