Voltage-gated potassium (Kv) channels couple with cytoplasmic ß-subunits (Kvß) that exhibit aldo-keto reductase (AKR) activity. Kvß subunits typically have exceptionally low catalytic turnover making them slow substrate converters. This poses a conundrum: why would an ion channel be shackled with a subpar enzyme? The AKR activity is crucial in Drosophila sleep regulation in dorsal fan-shaped body neurons (dFBN) where the Kv1 family member, Shaker, is paired with the ß-subunit Hyperkinetic. We show that its low catalytic turnover permits Hyperkinetic to monitor and integrate cumulative oxidative stress as a biochemical memory in a reversible voltage dependent manner. This functionality is harnessed by the Drosophila sleep homeostat to integrate oxidative stress and promote sleep before harmful levels are reached and, in the process, erase this memory to reset the system. Hyperkinetic represents memory as the redox state of its bound NADPH cofactor where transient exposure to oxidative substrates forms persistent changes to the paired Shaker channel’s inactivation kinetics. This increases neural activity in dFBNs to promote sleep. We show that artificially elevating Hyperkinetic substrate load produces a nigh-constant sleep; an effect which is constrained to the dFBNs. Further, these substrates produce a concomitant alteration in Shaker kinetics in dFBNs when interrogated by in-vivo patch clamp. Crucially, these alterations are erased when applying protocols mimicking the high activity of dFBNs during sleep. This demonstrates a system where sleep promoting neurons monitor oxidative stress as biochemical memory to promote protective sleep by increasing neuronal activity, and this neuronal activity itself resets that memory.