Bats are reservoirs for emerging human pathogens, including Hendra and Nipah henipaviruses and Ebola and Marburg filoviruses. These viruses demonstrate predictable patterns in seasonality and age structure across multiple systems; previous work suggests that they may circulate in Madagascar's endemic fruit bats, which are widely consumed as human food. We aimed to (a) document the extent of henipa‐ and filovirus exposure among Malagasy fruit bats, (b) explore seasonality in seroprevalence and serostatus in these bat populations and (c) compare mechanistic hypotheses for possible transmission dynamics underlying these data. To this end, we amassed and analysed a unique dataset documenting longitudinal serological henipa‐ and filovirus dynamics in three Madagascar fruit bat species. We uncovered serological evidence of exposure to Hendra‐/Nipah‐related henipaviruses in Eidolon dupreanum, Pteropus rufus and Rousettus madagascariensis, to Cedar‐related henipaviruses in E. dupreanum and R. madagascariensis and to Ebola‐related filoviruses in P. rufus and R. madagascariensis. We demonstrated significant seasonality in population‐level seroprevalence and individual serostatus for multiple viruses across these species, linked to the female reproductive calendar. An age‐structured subset of the data highlighted evidence of waning maternal antibodies in neonates, increasing seroprevalence in young and decreasing seroprevalence late in life. Comparison of mechanistic epidemiological models fit to these data offered support for transmission hypotheses permitting waning antibodies but retained immunity in adult‐age bats. Our findings suggest that bats may seasonally modulate mechanisms of pathogen control, with consequences for population‐level transmission. Additionally, we narrow the field of candidate transmission hypotheses by which bats are presumed to host and transmit potentially zoonotic viruses globally.