The straw-coloured fruit bat, Eidolon helvum, has been identified as a reservoir for potentially-zoonotic henipaviruses and Lagos bat virus (LBV) in continental Africa. Longitudinal studies at a large urban colony in Accra, Ghana aim to better understand E. helvum and viral ecology, as well as the nature of human-bat interactions. To assess whether the findings from these studies can be extrapolated across the species’ continental range, more information on the movement ecology of the species and connectivity of populations across its range was required. A multifaceted approach, using techniques from the field of genetics, population ecology, and virology, was used to understand the ways in which the structure and dynamics of fruit bat populations across Africa may affect the viral transmission dynamics within them. Given recent difficulties in using electronic positioning systems on E. helvum to track movement, genetic methods were proposed as the most appropriate way to assess connectivity between populations across such a vast range. Henipavirus and LBV serological analyses were undertaken on samples from 12 populations of E. helvum bats across its continental and offshore-island range. A combination of mitochondrial DNA and microsatellite markers were used to describe the genetic metapopulation structure of E. helvum and data were obtained in each location on population sizes, demographic structure, reproductive and migratory seasonality, as well as bat-human interactions. Consistent with expectations for a vagile migratory species, a panmictic continental population structure was detected across its continental range, although the extent of this panmixia was greater than previously detected in any other mammal or bird. Antibodies to henipaviruses and LBV were detected in all continental populations. Isolated island populations in the Gulf of Guinea were genetically distinct from each other and the continental population. Given the isolation of these island fruit bats and the lack of connectivity with other populations, it was expected that populations would be too small to allow persistence of any viruses that cause acute, immunising infections. Contrary to expectations, island individuals displayed evidence for exposure to both viruses. E. helvum is known to roost close in proximity to human populations across continental Africa, and these results could therefore have important public health implications. Further longitudinal studies across multiple locations and information on social structure, daily and seasonal movements are needed to make inferences about virus transmission dynamics and zoonotic risks within the complex population structure.