The quality of the adaptive immune response depends on the differentiation of distinct CD4⁺ helper T cell subsets, and the magnitude of an immune response is controlled by CD4⁺Foxp3⁺ regulatory T cells (T_reg cells). However, how a tissue- and cell type–specific suppressor program of T_reg cells is mechanistically orchestrated has remained largely unexplored. Through the use of T_reg cell–specific gene targeting, we found that the suppression of allergic immune responses in the lungs mediated by T helper type 2 (T_H2) cells was dependent on the activity of the protein kinase CK2. Genetic ablation of the β-subunit of CK2 specifically in T_reg cells resulted in the proliferation of a hitherto-unexplored ILT3⁺ T_reg cell subpopulation that was unable to control the maturation of IRF4⁺PD-L2⁺ dendritic cells required for the development of T_H2 responses in vivo.