How are sensory representations in the brain influenced by the state of an animal? Here we use chronic two-photon calcium imaging to explore how wakefulness and experience shape odor representations in the mouse olfactory bulb. Comparing the awake and anesthetized state, we show that wakefulness greatly enhances the activity of inhibitory granule cells and makes principal mitral cell odor responses more sparse and temporally dynamic. In awake mice, brief repeated odor experience leads to a gradual and long-lasting (months) weakening of mitral cell odor representations. This mitral cell plasticity is odor specific, recovers gradually over months, and can be repeated with different odors. Furthermore, the expression of this experience-dependent plasticity is prevented by anesthesia. Together, our results demonstrate the dynamic nature of mitral cell odor representations in awake animals, which is constantly shaped by recent odor experience. Display omitted ► Wakefulness makes mitral cell odor representations sparser, dynamic, and efficient ► Wakefulness enhances inhibitory granule cell activity ► Odor experience causes months-long, odor-specific changes of mitral cell tuning ► The expression of mitral cell experience-dependent plasticity requires wakefulness How are brain sensory representations influenced by the state of an animal? Kato et al. use chronic two-photon calcium imaging to show that in the awake mouse olfactory bulb, odor representations are sparse and dynamic due to increased interneuron activity and are shaped by recent experience.