The optical design of most insect apposition compound eyes should restrict activity to daylight because at night the tiny lenses of the isolated ommatidia cannot collect sufficient light. However, several bee species have adopted nocturnal activity, taking advantage of the benefits of night foraging. By measuring behavioural visual performance in honeybees, we show that insects can possess better spatial resolution in dim light than the optics and physiology of their apposition eyes suggest, implying the presence of higher neural mechanisms which enhance vision at night. Theoretical calculations reveal that honeybees improve light capture at night by neurally summing photons in space and time. Even though summation compromises both spatial and temporal resolution, the improved photon capture enhances vision sufficiently for bees to discriminate coarse images in moonlight. This explains how bees and many other insects can adopt a nocturnal lifestyle despite having an eye design typical of a day-active insect.