The interplay between effector T cells and regulatory T cells (T_reg cells) is crucial for adaptive immunity, but how T_reg cells control diverse effector responses is elusive. We found that the phosphatase PTEN links T_reg cell stability to repression of type 1 helper T cell (T_H1 cell) and follicular helper T cell (T_FH cell) responses. Depletion of PTEN in T_reg cells resulted in excessive T_FH cell and germinal center responses and spontaneous inflammatory disease. These defects were considerably blocked by deletion of interferon-γ, indicating coordinated control of T_H1 and T_FH responses. Mechanistically, PTEN maintained T_reg cell stability and metabolic balance between glycolysis and mitochondrial fitness. Moreover, PTEN deficiency upregulates activity of the metabolic checkpoint kinase complex mTORC2 and the serine-threonine kinase Akt, and loss of this activity restores functioning of PTEN-deficient T_reg cells. Our studies establish a PTEN-mTORC2 axis that maintains T_reg cell stability and coordinates T_reg cell–mediated control of effector responses.