Barrier tissues, like the skin, are sites where noninvasive commensal microbes constantly interact with resident T cells. These encounters can result in commensal-specific T cell responses that promote, for example, host defense and tissue repair. Harrison et al. show that subsets of skin-resident commensal-specific interleukin-17A–producing CD4+ and CD8+ T cells have a dual nature: They coexpress transcription factors that direct antagonistic antimicrobial (type 17) and antiparasite and pro–tissue repair (type 2) programs. When skin is damaged, epithelial cell alarmins license type 17 T cells to turn on type 2 cytokines. Thus, commensal-specific type 17 T cells can direct antimicrobial activity under homeostatic conditions but rapidly turn on tissue repair in the context of injury.