Long recognized to be potent suppressors of immune responses, Foxp3+CD4+ regulatory T (Treg) cells are being rediscovered as regulators of nonimmunological processes. We describe a phenotypically and functionally distinct population of Treg cells that rapidly accumulated in the acutely injured skeletal muscle of mice, just as invading myeloid-lineage cells switched from a proinflammatory to a proregenerative state. A Treg population of similar phenotype accumulated in muscles of genetically dystrophic mice. Punctual depletion of Treg cells during the repair process prolonged the proinflammatory infiltrate and impaired muscle repair, while treatments that increased or decreased Treg activities diminished or enhanced (respectively) muscle damage in a dystrophy model. Muscle Treg cells expressed the growth factor Amphiregulin, which acted directly on muscle satellite cells in vitro and improved muscle repair in vivo. Thus, Treg cells and their products may provide new therapeutic opportunities for wound repair and muscular dystrophies. Display omitted •Treg cells of a distinct phenotype accumulate in injured murine skeletal muscle•Muscle Treg cells also accumulate in mouse models of muscular dystrophy•Treg cells control muscle inflammation upon injury and promote muscle repair•Amphiregulin, made by muscle Tregs, boosts satellite cell function and muscle repair A unique population of Treg cells accumulate in acutely or chronically injured skeletal muscle to promote muscle repair by controlling both immune and nonimmune cells.