Foxp3⁺ regulatory T cells (T_reg cells) maintain immunological tolerance, and their deficiency results in fatal multiorgan autoimmunity. Although heightened signaling via the T cell antigen receptor (TCR) is critical for the differentiation of T_reg cells, the role of TCR signaling in T_reg cell function remains largely unknown. Here we demonstrated that inducible ablation of the TCR resulted in T_reg cell dysfunction that could not be attributed to impaired expression of the transcription factor Foxp3, decreased expression of T_reg cell signature genes or altered ability to sense and consume interleukin 2 (IL-2). Instead, TCR signaling was required for maintaining the expression of a limited subset of genes comprising 25% of the activated T_reg cell transcriptional signature. Our results reveal a critical role for the TCR in the suppressor capacity of T_reg cells.