T regulatory cells that express the transcription factor Foxp3 (Foxp3⁺ T_regs) promote tissue homeostasis in several settings. We now report that symbiotic members of the human gut microbiota induce a distinct T_reg population in the mouse colon, which constrains immuno-inflammatory responses. This induction—which we find to map to a broad, but specific, array of individual bacterial species—requires the transcription factor Rorγ, paradoxically, in that Rorγ is thought to antagonize FoxP3 and to promote T helper 17 (T_H17) cell differentiation. Rorγ’s transcriptional footprint differs in colonic T_regs and T_H17 cells and controls important effector molecules. Rorγ, and the T_regs that express it, contribute substantially to regulating colonic T_H1/T_H17 inflammation. Thus, the marked context-specificity of Rorγ results in very different outcomes even in closely related cell types.