IL-33 promotes regulatory T cell (Treg) function in the intestine. This study shows that the IL-33 receptor ST2 is preferentially expressed on colonic Treg cells, where it enhances Treg function and adaptation to inflammatory environments. IL-33 signaling stimulates Treg responses by enhancing TGF-β1-mediated differentiation and supporting Treg accumulation and maintenance in inflamed tissues. IL-23, a key pro-inflammatory cytokine in inflammatory bowel disease (IBD), inhibits Treg responses by suppressing IL-33 responsiveness. These findings suggest a novel link between an endogenous damage signal and an anti-inflammatory pathway, with the balance between IL-33 and IL-23 playing a key role in intestinal immune responses. ST2 is highly expressed in colonic Treg cells, and its expression is regulated by GATA3. IL-33 activates GATA3 in Treg cells, promoting ST2 expression and enhancing Treg function. IL-33 also promotes its own receptor expression in Treg cells, creating an amplification loop that enhances Treg differentiation. IL-33 promotes Treg proliferation and accumulation in vivo, particularly in thymus-derived Treg cells. In chronic colitis models, IL-33 levels increase in the colon, and soluble ST2 (sST2) is elevated, which may limit IL-33 bioavailability and antagonize its activity. However, IL-33 signaling in Treg cells is essential for their suppressive function in vivo. IL-23 inhibits the effects of IL-33 on Treg cells by limiting their responsiveness to IL-33. This inhibition is mediated through the regulation of T cell responsiveness to IL-33, which is crucial for Treg differentiation. IL-23 also inhibits the expression of GATA3 and ST2, which are essential for Treg function. The balance between IL-33 and IL-23 is therefore a key determinant of intestinal immune responses. The study identifies a new function for IL-33 as a critical link between inflammation-driven tissue damage and the local intestinal Treg response. IL-33 signaling through ST2 in Treg cells is essential for their ability to adapt to the inflammatory environment and control intestinal inflammation. The ability of IL-33 to amplify regulatory networks in response to tissue injury may represent a general mechanism by which alarmins limit immune-mediated damage to self at barrier tissues. IL-23 limits this regulatory mechanism by inhibiting Treg cell responsiveness to IL-33, suggesting that the balance between IL-23 and IL-33 is a major determinant of the outcome of intestinal immune responses.IL-33 promotes regulatory T cell (Treg) function in the intestine. This study shows that the IL-33 receptor ST2 is preferentially expressed on colonic Treg cells, where it enhances Treg function and adaptation to inflammatory environments. IL-33 signaling stimulates Treg responses by enhancing TGF-β1-mediated differentiation and supporting Treg accumulation and maintenance in inflamed tissues. IL-23, a key pro-inflammatory cytokine in inflammatory bowel disease (IBD), inhibits Treg responses by suppressing IL-33 responsiveness. These findings suggest a novel link between an endogenous damage signal and an anti-inflammatory pathway, with the balance between IL-33 and IL-23 playing a key role in intestinal immune responses. ST2 is highly expressed in colonic Treg cells, and its expression is regulated by GATA3. IL-33 activates GATA3 in Treg cells, promoting ST2 expression and enhancing Treg function. IL-33 also promotes its own receptor expression in Treg cells, creating an amplification loop that enhances Treg differentiation. IL-33 promotes Treg proliferation and accumulation in vivo, particularly in thymus-derived Treg cells. In chronic colitis models, IL-33 levels increase in the colon, and soluble ST2 (sST2) is elevated, which may limit IL-33 bioavailability and antagonize its activity. However, IL-33 signaling in Treg cells is essential for their suppressive function in vivo. IL-23 inhibits the effects of IL-33 on Treg cells by limiting their responsiveness to IL-33. This inhibition is mediated through the regulation of T cell responsiveness to IL-33, which is crucial for Treg differentiation. IL-23 also inhibits the expression of GATA3 and ST2, which are essential for Treg function. The balance between IL-33 and IL-23 is therefore a key determinant of intestinal immune responses. The study identifies a new function for IL-33 as a critical link between inflammation-driven tissue damage and the local intestinal Treg response. IL-33 signaling through ST2 in Treg cells is essential for their ability to adapt to the inflammatory environment and control intestinal inflammation. The ability of IL-33 to amplify regulatory networks in response to tissue injury may represent a general mechanism by which alarmins limit immune-mediated damage to self at barrier tissues. IL-23 limits this regulatory mechanism by inhibiting Treg cell responsiveness to IL-33, suggesting that the balance between IL-23 and IL-33 is a major determinant of the outcome of intestinal immune responses.