Mucosal-associated invariant T (MAIT) cells are the most abundant unconventional T cells in the lung and have a recently-described function in maintaining tissue homeostasis, indicating their potential role in promoting pulmonary tissue repair. It is not known what role MAIT cells play during sterile tissue damage, or the functional consequences of their tissue repair capabilities in the lung. Using a bleomycin-induced murine lung injury model, we show in vivo that bleomycin challenge strongly activated murine pulmonary MAIT cells and induced their tissue repair program. MAIT cell-deficient Mr1-/- mice exhibited more severe weight loss and a more robust immune response following bleomycin challenge compared with their wild-type counterparts. We further demonstrate that early accumulation of CD103+ type 1 dendritic cell (cDC1) in the lungs of Mr1-/- mice was impaired upon bleomycin challenge, and MAIT cells were required for the early differentiation of CCR2+ Ly6Chi monocytes into cDC1. Finally, the weight loss of Mr1-/- mice was rescued by adoptive transfer of bone marrow-derived dendritic cells (BMDCs) but this effect was lost when DNGR-1 was blocked in the mice. Overall, our data suggested that MAIT cells played a protective role against bleomycin-induced lung tissue damage by promoting monocyte differentiation into cDC1, which limited tissue damage via the DNGR-1 signal. These findings establish a novel mechanism by which MAIT cells function to reduce damage during sterile tissue injury and provide insight into the potential use of MAIT cells in pulmonary tissue repair.