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Zbtb20<jats:sup>+<\/jats:sup>T<jats:sub>regs<\/jats:sub>were phenotypically and genetically distinct from the larger conventional T<jats:sub>reg<\/jats:sub>population. Zbtb20<jats:sup>+<\/jats:sup>T<jats:sub>regs<\/jats:sub>constitutively expressed mRNA for interleukin-10 and produced high levels of the cytokine upon primary activation. Zbtb20<jats:sup>+<\/jats:sup>T<jats:sub>regs<\/jats:sub>were enriched in the intestine and specifically expanded when inflammation was induced by the use of dextran sodium sulfate. Conditional deletion of<jats:italic>Zbtb20<\/jats:italic>in T cells resulted in a loss of intestinal epithelial barrier integrity. Consequently, knockout (KO) mice were acutely sensitive to colitis and often died because of the disease. Adoptive transfer of Zbtb20<jats:sup>+<\/jats:sup>T<jats:sub>regs<\/jats:sub>protected the Zbtb20 conditional KO mice from severe colitis and death, whereas non-Zbtb20 T<jats:sub>regs<\/jats:sub>did not. Zbtb20 was detected in CD24<jats:sup>hi<\/jats:sup>double-positive and CD62L<jats:sup>lo<\/jats:sup>CD4 single-positive thymocytes, suggesting that expression of the transcription factor and the phenotype of these cells were induced during thymic development. However, Zbtb20 expression was not induced in \u201cconventional\u201d T<jats:sub>regs<\/jats:sub>by activation in vitro or in vivo. 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