Nearly all organisms evolved with natural light-dark rhythms, making light a key sensory cue for regulating behaviour. Seasonal and daily variation in light-dark rhythms provide timing cues for long-distance avian migrants, and nocturnal migrants also require natural light at night to navigate visually during migration. Natural light cues have been disrupted by the rapid growth of artificial light within the migratory landscape, affecting the timing and movements of many nocturnally migrating birds. Research has focussed on diurnal species that migrate at night, leaving open questions about how obligate nocturnal bird species, which are highly sensitive to light, respond to variation in light at night during migration. I used an obligate nocturnal bird, the Eastern Whip-poor-will (Antrostomus vociferous), to explore how natural daylight, the lunar cycle, and artificial light influence migration movements in a nocturnal species. I GPS-tracked Whip-poor-wills during their fall migrations between Canada and Central America to generate the highest resolution migration data yet for this species. I found that Whip-poor-will migration timing followed natural light-dark rhythms, which implies potential limitations to flexibility in migration timing. Daily flights were restricted to dark hours, contradicting theory about optimal time management that has generally been supported by evidence from diurnal species. Whip-poor-wills synchronized their fall departures around the full moon, supporting the hypothesis that full-moon foraging facilitates fuel deposition in preparation for migration. Birds from different breeding locations appeared to adjust migration timing differently in anticipation of a late-season full moon, although individuals maintained remarkably repeatable departure dates across years. I also found some of the first evidence for artificial light avoidance in migrating birds: Whip-poor-wills avoided brightly lit urban areas during migratory flights, and especially during stopovers. Finally, I demonstrated that Whip-poor-wills undergo a leap-frog migration to maintain migratory connectivity. This result can inform tailored conservation plans for specific groups of birds that encounter different threats, such as artificial light, between their breeding and non-breeding grounds. Overall, my research resolved some of the mystery around this understudied, at-risk species, and provided a foundation for more nuanced hypotheses about the endogenous and environmental light cues that control nocturnal species’ migration movements.