Regulatory T-cells (Tregs) play a dual role in colon cancer, promoting immune tolerance and suppressing inflammation. We have observed two types of Tregs in patients with colon, lung, and pancreatic cancer. The subset that preferentially expands in these patients has pro-inflammatory properties and express RORgt. Using mouse models, we showed that expression of RORgt is controlled by b-catenin. Tregs and CD4+ T-cells from colon cancer had elevated expression of b-catenin. To test the role of canonical Wnt signaling in the generation of pro-inflammatory Tregs, we stabilized β-catenin or deleted its DNA binding partner TCF-1 in Tregs. In both instances’ expression of RORγt was upregulated. While the stabilization of β-catenin led to loss of Treg functions, ablation of TCF-1 reproduced the phenotype and functional characteristics of Tregs in colon cancer. The TCF-1 deficient Tregs were pro-inflammatory, potent T-cell suppressive, and tumor promoting. Therefore, we were able to reproduce the phenotype and functions of Tregs in colon cancer patients. Expansion of this subset of Tregs is responsible for deregulation of tumor promoting Th17 inflammation in colon cancer.