Although it is well established that microbial infections predispose to autoimmune diseases, the underlying mechanisms remain poorly understood. After infection, tissue-resident memory T (T_RM) cells persist in peripheral organs and provide immune protection against reinfection. However, whether T_RM cells participate in responses unrelated to the primary infection, such as autoimmune inflammation, is unknown. By using high-dimensional single-cell analysis, we identified CD4⁺ T_RM cells with a T_H17 signature (termed T_RM17 cells) in kidneys of patients with ANCA-associated glomerulonephritis. Experimental models demonstrated that renal T_RM17 cells were induced by pathogens infecting the kidney, such as <i>Staphylococcus aureus</i>, <i>Candida albicans</i>, and uropathogenic <i>Escherichia coli</i>, and persisted after the clearance of infections. Upon induction of experimental glomerulonephritis, these kidney T_RM17 cells rapidly responded to local proinflammatory cytokines by producing IL-17A and thereby exacerbate renal pathology. Thus, our data show that pathogen-induced T_RM17 cells have a previously unrecognized function in aggravating autoimmune disease.