Naïve T cells are typically considered to be in a default state of quiescence, whereas memory T cells undergo basal proliferation and quickly exhibit effector responses when stimulated. Over the past few years, however, a more complex picture has emerged, with evidence that naïve T cell quiescence is actively enforced, and that heterogeneity among naïve T cells influences their capacity to escape quiescence in response to homeostatic cues. Furthermore, the active state of memory T cells may also be instructed, requiring contact with dendritic cells to avoid reversion to quiescence. Here, we discuss these new findings and propose that there is much more flexibility in the quiescent state of naïve and memory T cells than previously thought.