Although regulatory T cells (T_regs) are known to suppress self-reactive autoimmune responses, their role during T cell responses to nonself antigens is not well understood. We show that T_regs play a critical role during the priming of immune responses in mice. T_reg depletion induced the activation and expansion of a population of low-avidity CD8⁺ T cells because of overproduction of CCL-3/4/5 chemokines, which stabilized the interactions between antigen-presenting dendritic cells and low-avidity T cells. In the absence of T_regs, the avidity of the primary immune response was impaired, which resulted in reduced memory to Listeria monocytogenes. These results suggest that T_regs are important regulators of the homeostasis of CD8⁺ T cell priming and play a critical role in the induction of high-avidity primary responses and effective memory.