Capsiate is known to increase whole body oxygen consumption possibly via the activation of uncoupling processes, but its effect at skeletal muscle level remains poorly documented and conflicting. To clarify this issue, gastrocnemius muscle function and energetics were investigated in mice, 2 hours after a single intake of either vehicle (control) or purified capsiate (at 10- or 100-mg/kg body weight), through a multidisciplinary approach combining in vivo and in vitro measurements. Mechanical performance and energy pathway fluxes were accessed strictly noninvasively during a standardized electrostimulation-induced exercise using an original device implementing 31-phosphorus magnetic resonance spectroscopy, and mitochondrial respiration was evaluated in isolated saponin-permeabilized fibers. Compared to control, both capsiate doses produced quantitatively similar effects at the energy metabolism level, including an about 2-fold decrease of the mitochondrial respiration sensitivity for ADP. Interestingly, they did alter neither oxidative phosphorylation nor uncoupling protein 3 gene expression at rest. During 6-min of maximal repeated isometric contractions, both doses reduced the amount of ATP produced from glycolysis and oxidative phosphorylation, but increased the relative contribution of oxidative phosphorylation to total energy turnover (+28% and +21% in 10-mg and 100-mg groups, respectively). ATP cost of contraction was further reduced in 10-mg (-35%) and 100-mg (-45%) groups. Besides, the highest dose also increased the force-generating capacity. These data present capsiate as a helpful candidate to enhance both muscle performance and oxidative phosphorylation during exercise, which could constitute a nutritional approach for improving health and preventing obesity and associated metabolic disorders.