The evolutionary purpose of sleep is an enduring biological mystery of the animal kingdom. Most research to date has investigated the processes that occur during sleep as opposed to why it evolved in the first place, and a recent theory proposes this behavior evolved to restrict activity to one temporal niche. Circadian rhythms are intimately linked to sleep, and in derived species, sleep-wake behaviors have been well characterized and are regulated by neuronal circuits. However, recent studies suggest sleep is also present in species lacking a centralized nervous system, and in this review, we discuss the interplay between ancient circadian processes and their potential role in the evolution of sleep behavior. By approaching the evolution of sleep using a comparative physiology perspective, we present evidence that layers of molecular oscillators and highly conserved sleep signaling molecules predate neurons, and sleep is a fundamentally ancient process.