The role of regulatory T cells (T_regs) in human colon cancer (CC) remains controversial: high densities of tumor-infiltrating T_regs can correlate with better or worse clinical outcomes depending on the study. In mouse models of cancer, T_regs have been reported to suppress inflammation and protect the host, suppress T cells and protect the tumor, or even have direct cancer-promoting attributes. These different effects may result from the presence of different T_reg subsets. We report the preferential expansion of a T_reg subset in human CC with potent T cell–suppressive, but compromised anti-inflammatory, properties; these cells are distinguished from T_regs present in healthy donors by their coexpression of Foxp3 and RORγt. T_regs with similar attributes were found to be expanded in mouse models of hereditary polyposis. Indeed, ablation of the RORγt gene in Foxp3⁺ cells in polyp-prone mice stabilized T_reg anti-inflammatory functions, suppressed inflammation, improved polyp-specific immune surveillance, and severely attenuated polyposis. Ablation of interleukin-6 (IL-6), IL-23, IL-17, or tumor necrosis factor–α in polyp-prone mice reduced polyp number but not to the same extent as loss of RORγt. Surprisingly, loss of IL-17A had a dual effect: IL-17A–deficient mice had fewer polyps but continued to have RORγt⁺ T_regs and developed invasive cancer. Thus, we conclude that RORγt has a central role in determining the balance between protective and pathogenic T_regs in CC and that T_reg subtype regulates inflammation, potency of immune surveillance, and severity of disease outcome.