Coupling between cyclically varying external light and an endogenous biochemical oscillator known as the circadian clock, modulates a rhythmic pattern with two prominent peaks in the locomotion of Drosophila melanogaster. A morning peak appears around the time lights turn on and an evening peak appears just before lights turn off. The close association between the peaks and the external 12:12 hour light/dark photoperiod means that respective morning and evening peaks of individual flies are well-synchronized in time and, consequently, feature prominently in population-averaged data. Here, we report on a brief but strong stochastic burst in fly activity that, in contrast to morning and evening peaks, is detectable only in single fly recordings. This burst was observed across 3 wild-type strains of Drosophila melanogaster. In a single fly recording, the burst is likely to appear once randomly within 0.5-5 hours after lights turn on, last for only 2-3 minutes and yet show 5 times greater activity compared to the maximum of morning peak with data binned in 3 minutes. Owing to its variable timing and short duration, the burst is virtually undetectable in population-averaged data. We use a locally-built illumination system to study the burst and find that its incidence in a population correlates with light intensity, with ~85% of control flies showing the behavior at 8000 lux (1942 μW/cm2). Consistent with that finding, several mutant flies with impaired vision show substantially reduced frequency of the burst. Additionally, we find that genetic ablation of the clock has insignificant effect on burst frequency. Together, these data suggest that the pronounced burst is likely generated by a light-activated circuit that is independent of the circadian clock.