Mammalian barrier tissues are constitutively colonized by numerous microorganisms. We explored how these microbes were sensed by the immune system, specifically how T cell responses to these microbes influenced skin physiology. Our studies identified that a skin commensal can induce T cell responses in the absence of inflammation in a manner dependent upon non-classical MHC class I molecules. Developing tools to track commensal-specific T cells in the skin demonstrated their role as long-lived sentinels of skin tissue, in part by adopting a distinct transcriptional state, that both promoted defense against skin infection and accelerated skin wound repair. Our work highlights immunity to commensal microbes as a key contributor to barrier tissue homeostasis and repair..