Specialized tissues demand support for long-term fitness. In the heart, for example, the removal of spent mitochondria by macrophages is critical for cardiac function. In an organismal-wide screening, we show here that the transfer of mitochondria to macrophages is prominent in other organs that rely on mitochondrial respiration, including the skeletal muscle and brown adipose tissue (BAT). Depletion of macrophages altered the mitochondrial activity and compromised the mechanical and thermogenic performance of these organs. Using comparative, genetic and surgical approaches, we show that the abundance of macrophages in a muscle is dictated by the mitochondrial activity of its myofibers, and that this is achieved by modulating the number of Csf1-producing fibroblasts in the tissue. Consequently, inhibition of the Csf1 receptor collapsed the mitochondrial activity of skeletal muscles. Thus, by regulating the abundance of macrophages, tissues enact an adaptive mechanism that copes with high mitochondrial turnover and supports their function.