The social structure of animal aggregations may vary considerably in both space and time, yet little is known about how this affects vigilance. Here, we investigate the vigilance architecture of a colony of wild-living grey-headed flying-foxes (Pteropus poliocephalus) in Australia and examine how spatial as well as temporal variation in social organization influences social and environmental vigilance. We sampled color-marked individuals at different stages of the reproductive cycle and the year and at different locations in the colony to examine the effects of temporal and spatial factors on social and environmental vigilance. We found that vigilance architecture reflected the social structure of the colony, with the highest environmental vigilance being displayed by bats at the periphery of the colony, and the highest social vigilance by bats that roosted at intermediate distances from the colony’s edge. Furthermore, we found that vigilance levels reflected changes in reproductive state, with social vigilance increasing toward the mating season, particularly in males. Our findings show that spatial and temporal variation in social structure can have differential effects on social and environmental vigilance. This highlights the necessity to differentiate between functions of vigilance to understand fully vigilance architecture in aggregations of social animals.