Abstract Foxp3+T regulatory (Treg) cells are crucial to maintain immune homeostasis both in lymphoid and non-lymphoid tissues. Here we demonstrate that the ability of intestinal Treg cells to constrain microbiota-dependent interleukin 17–producing T helper cell (TH17) and immunoglobulin A (IgA) responses critically required the expression of the transcription factor c-Maf. The terminal differentiation and function of several intestinal Treg cell populations, including RORgt+Tregcells and T follicular regulatory cells, was c-Maf-dependent. c-Maf controlled Treg cell-derived interleukin 10 (IL-10) production and prevented excessive phosphatidylinositol-3-OH kinase (PI(3)K)–kinase Akt–mechanistic target of rapamycin (mTORC1) signaling and inflammatory cytokine expression in intestinal Treg cells. c-Maf-deficiency in Treg cells led to a profound dysbiosis of the intestinal microbiota, which when transferred to germ-free mice, was sufficient to induce exacerbated intestinal TH17 responses, even in a c-Maf-competent environment. Thus, c-Maf acts to preserve the identity and function of intestinal Treg cells, which is essential for the establishment of host-microbial symbiosis.