When females and males differ in their timing of maximum reproductive effort, this can result in sex-specific seasonal cycles in body mass. Such cycles are undoubtedly under strong selection, particularly in bats, where they affect flying ability. Flying foxes (Old World fruit bats, Pteropus spp.) are the largest mammals that can sustain powered flight and therefore face critical trade-offs in managing body reserves for reproduction, yet little is known about body mass dynamics in this group. I investigated body mass changes in relation to reproductive behaviour in a large colony of grey-headed flying foxes (Pteropus poliocephalus). In this polygynous mammal, females were predicted to maximise reproductive effort during lactation and males during the breeding season. As predicted, female body condition declined during the nursing period, but did not vary in relation to sexual activity. By contrast, males accumulated body reserves prior to the breeding season, but subsequently lost over 20% of their body mass on territory defence and courtship, and lost foraging opportunities as they also defended their day roost territories at night. Males in better condition had larger testes, particularly during territory establishment, prior to maximum sexual activity. Thus, the seasonality of female mass reflected the high metabolic load that lactation imposes on mothers. However, male mass followed a pattern akin to the "fatted male phenomenon", which is commonly observed in large polygynous mammals with seasonal reproduction, but not in bats. This shows the importance of body reserves for reproduction in flying foxes, despite their severe constraints on body mass.