Homeostatic mechanisms stabilize neural circuit function by keeping firing rates (FRs) within a set-point range, but whether individual neocortical neurons regulate firing cell-autonomously, and whether this process is restricted to certain behavioral states such as sleep or wake, is unknown. We have followed the process of FR homeostasis in individual visual cortical neurons in freely behaving rodents as they cycled between sleep and wake states. When FRs are perturbed by visual deprivation, over time they return precisely to a cell-autonomous set-point, and this restoration of firing occurs selectively during periods of active waking and is suppressed by sleep. Longer natural waking periods result in more FR homeostasis, as does artificially extending the length of waking. This exclusion of FR homeostasis from sleep raises the possibility that memory consolidation or some other sleep-dependent process is vulnerable to interference from homeostatic plasticity mechanisms.