Primates spend on average half as much energy as other placental mammals while expressing a wide range of lifestyles. However, little is known about how primates adapt their rate of energy use in the context of natural environmental variations. Using doubly labelled water, behavioral and accelerometric methods, we measured the total energy expenditure (TEE) and body composition of a population of Eulemur fulvus (N = 12) living in an agroforest in Mayotte. We show that the TEE of this medium-sized cathemeral primate is one of the lowest recorded to date in eutherians. Regression models show that individual variation in the rate of energy use is predicted by fat-free mass, body size, thigh thickness and maximum temperature. TEE is positively correlated with increasing temperature, suggesting that thermoregulation is an important component of the energy budget of this frugivorous species. Mass-specific TEE is only 10% lower than that of a closely related species previously studied in a gallery forest, consistent with the assertion that TEE varies within narrow physiological limits. As lemur communities include many species with unique thermoregulatory adaptations, circadian and/or seasonal temperature variations may have constituted a major selective pressure on the evolution of lemur metabolic strategies.