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Sleep is ubiquitous across the animal kingdom. However, the definition for sleep varies significantly across species. In organisms such as C. elegans, Drosophila, and zebrafish, sleep is classically defined as periods of locomotor quiescence with an increased arousal threshold^–. In mammals, sleep is further subdivided into rapid eye movement (REM) and non-rapid eye movement (NREM) sleep, but the evolutionary origin of these two sleep states remains unclear^–. Using longitudinal, high-resolution imaging of naturalistic sleep-wake behavior, we find that the classical definition of larval zebrafish sleep encompasses two clearly distinct quiescent states, one with rapid eye movements (qREM) and one without rapid eye movements (qNREM). Remarkably, qREM states are maintained in congenitally blind larval zebrafish, suggesting that qREM emerged during vertebrate evolution not as a response to internally generated visual imagery (i.e., the “scanning hypothesis”), but potentially as a strategy to maintain oculomotor stimulation during rest. Lastly, using brain-wide imaging in freely swimming animals, we find that, in contrast to fixed point attractor models of sleep developed in invertebrates, population-level activity during zebrafish qREM unfolds along smooth committed trajectories through state-space. This work suggests a significant rethinking of the behavioral and neural organization of sleep in early vertebrates and the emergence of REM during vertebrate evolution.