The population dynamics that enable a small number of regulatory T (T R) cells to control the immune responses to foreign Ags by the much larger conventional T cell subset were investigated. During the primary immune response, the expansion and contraction of conventional and T R cells occurred in synchrony. Importantly, the relative accumulation of T R cells at peak response significantly exceeded that of conventional T cells, reflecting extensive cell division within the T R cell pool. Transfer of a polyclonal T R cell population before immunization antagonized both polyclonal and TCR transgenic responses, whereas blocking T R cell function enhanced those responses. These results define an inverse quantitative relationship between T R and conventional T cells that controls the magnitude of the primary immune response. The high frequency of dividing T R cells suggests degenerate TCR specificity enabling activation by a broad spectrum of Ags.