Several subsets of Foxp3⁺ regulatory T cells (T_reg cells) work in concert to maintain immune homeostasis. However, the molecular bases underlying the phenotypic and functional diversity of T_reg cells remain obscure. We show that in response to interferon-γ, Foxp3⁺ T_reg cells upregulated the T helper type 1 (T_H1)-specifying transcription factor T-bet. T-bet promoted expression of the chemokine receptor CXCR3 on T_reg cells, and T-bet⁺ T_reg cells accumulated at sites of T_H1 cell–mediated inflammation. Furthermore, T-bet expression was required for the homeostasis and function of T_reg cells during type 1 inflammation. Thus, in a subset of CD4⁺ T cells, the activities of the transcription factors Foxp3 and T-bet are overlaid, which results in T_reg cells with unique homeostatic and migratory properties optimized for the suppression of T_H1 responses in vivo.