The neural control of sleep requires that sleep need is sensed during waking and discharged during sleep. While sleep loss has widespread consequences in the whole body and brain, perhaps the only realistic opportunity for separating causation from correlation exists in specialist neurons with active roles in sleep. To obtain an unbiased view of molecular changes in the brain underlying these processes, we characterized the transcriptomes of single sleep-control cells isolated from rested and sleep-deprived flies. Transcripts upregulated after sleep deprivation, in sleep-control neurons projecting to the dorsal fan-shaped body (dFBNs) but not ubiquitously in the brain, encode almost exclusively proteins with roles in mitochondrial respiration and ATP synthesis. These changes are accompanied by mitochondrial fragmentation, enhanced mitophagy, and increased number of contacts between mitochondria and the endoplasmic reticulum. The morphological changes are reversible after recovery sleep and blunted by interfering at both ends of the electron transport chain, via the installation of an electron overflow in the chain or by consuming ATP via forced depolarisation. Inducing or preventing mitochondrial fission or fusion in dFBNs alters sleep and electrical properties of sleep-control cells bidirectionally: hyperfused mitochondria increase, whereas fragmented mitochondria decrease, neuronal excitability and sleep. ATP levels in dFBNs rise after enforced waking, because dopamine-mediated arousal diminishes their ATP consumption, predisposing them to heightened oxidative stress. Uncoupling electron flux from ATP synthesis relieves the pressure to sleep, while exacerbating mismatches between electron supply and ATP demand promotes sleep. Sleep control, like ageing, may thus be a consequence of aerobic metabolism.