Most T lymphocytes, including regulatory T cells (T_reg cells), differentiate in the thymus. The age-dependent involution of this organ leads to decreasing production of T cells. Here we found that the output of new T_reg cells from the thymus decreased substantially more than that of conventional T cells. Peripheral mouse and human T_reg cells recirculated back to the thymus, where they constituted a large proportion of the pool of T_reg cells and displayed an activated and differentiated phenotype. In the thymus, the recirculating cells exerted their regulatory function by inhibiting interleukin 2 (IL-2)-dependent de novo differentiation of T_reg cells. Thus, T_reg cell development is controlled by a negative feedback loop in which mature progeny cells return to the thymus and restrain development of precursors of T_reg cells.