Both microbial and host genetic factors contribute to the pathogenesis of autoimmune diseases^,,,. There is accumulating evidence that microbial species that potentiate chronic inflammation, as in inflammatory bowel disease, often also colonize healthy individuals. These microorganisms, including the Helicobacter species, can induce pathogenic T cells and are collectively referred to as pathobionts^,,. However, how such T cells are constrained in healthy individuals is not yet understood. Here we report that host tolerance to a potentially pathogenic bacterium, Helicobacter hepaticus, is mediated by the induction of RORγt⁺FOXP3⁺ regulatory T (iT_reg) cells that selectively restrain pro-inflammatory T helper 17 (T_H17) cells and whose function is dependent on the transcription factor c-MAF. Whereas colonization of wild-type mice by H. hepaticus promoted differentiation of RORγt-expressing microorganism-specific iT_reg cells in the large intestine, in disease-susceptible IL-10-deficient mice, there was instead expansion of colitogenic T_H17 cells. Inactivation of c-MAF in the T_reg cell compartment impaired differentiation and function, including IL-10 production, of bacteria-specific iT_reg cells, and resulted in the accumulation of H. hepaticus-specific inflammatory T_H17 cells and spontaneous colitis. By contrast, RORγt inactivation in T_reg cells had only a minor effect on the bacteria-specific T_reg and T_H17 cell balance, and did not result in inflammation. Our results suggest that pathobiont-dependent inflammatory bowel disease is driven by microbiota-reactive T cells that have escaped this c-MAF-dependent mechanism of iT_reg–T_H17 homeostasis.