Exercise is a nonpharmacological intervention that improves health during aging, and a valuable tool in the diagnostics of aging-related diseases. In muscle, exercise transiently alters mitochondrial functionality and metabolism. Mitochondrial fission and fusion are critical effectors of mitochondrial plasticity, which allows a fine-tuned regulation of organelle connectiveness, size and function. Here we have investigated the role of mitochondrial dynamics during exercise in the genetically tractable model Caenorhabditis elegans. We show that in body wall muscle a single exercise session induces a cycle of mitochondrial fragmentation followed by fusion after a recovery period, and that daily exercise sessions delay the mitochondrial fragmentation and fitness capacity decline that occur with aging. The plasticity of this mitochondrial dynamics cycle is essential for fitness capacity and its enhancement by exercise training. Surprisingly, among longevity-promoting mechanisms we analyzed, constitutive activation of AMPK uniquely preserves fitness capacity during aging. As with exercise training, this benefit of AMPK is abolished by impairment of mitochondrial fission or fusion. AMPK is also required for fitness capacity to be enhanced by exercise, with our findings together suggesting that exercise enhances muscle function through AMPK regulation of mitochondrial dynamics. Our results indicate that mitochondrial connectivity and the mitochondrial dynamics cycle are essential for maintaining fitness capacity and exercise responsiveness during aging, and suggest that AMPK activation may recapitulate some exercise benefits. Targeting mechanisms to optimize mitochondrial fission and fusion balance, as well as AMPK activation, may represent promising strategies for promoting muscle function during aging.