Sleep is an evolutionarily conserved yet still enigmatic behavioral state. Understanding the circuits underlying sleep–wake regulation is essential to elucidate the physiology of the sleeping brain. A key similarity between mammals and flies is homeostatic regulation: when deprived of sleep, flies exhibit a compensatory rebound the following day. Although the circadian pacemaker and the sleep homeostat can interact, the mechanisms remain poorly understood. In Drosophila, the circadian oscillator comprises ~250 neurons that express clock genes and generate transcriptional–translational feedback loops. Among them, the ventral lateral neurons (LNvs) are crucial for arousal and sleep–wake regulation, although their circuitry is not fully characterized. Historically, the small LNvs (sLNvs) were considered minor contributors to the sleep homeostat, despite their central role in circadian regulation. In this work, we investigated the role of sLNvs in sleep homeostasis. Manipulating the physiology of these neurons revealed a resistance to sleep deprivation, a previously unreported phenotype. Although sLNvs were not directly affected by mechanical deprivation, reducing inhibition onto these neurons induced robust resistance to sleep loss. These findings challenge current models and uncover an unexpected contribution of sLNvs to sleep homeostasis, opening new avenues for understanding the neuronal basis of sleep regulation.