Bats (order Chiroptera) have been increasingly recognised as important reservoir hosts for human and animal pathogens worldwide. In this context, molecular and microscopy-based investigations to date have revealed remarkably high diversity of Trypanosoma spp. harboured by bats, including species of recognised medical and veterinary importance such as Trypanosoma cruzi and Trypanosoma evansi (aetiological agents of Chagas disease and Surra, respectively). This review synthesises current knowledge on the diversity, taxonomy, evolution and epidemiology of bat trypanosomes based on both molecular studies and morphological records. In addition, we use a One Health approach to discuss the significance of bats as reservoirs (and putative vectors) of T. cruzi, with a focus on the complex associations between intra-specific genetic diversity and eco-epidemiology of T. cruzi in sylvatic and domestic ecosystems. This article also highlights current knowledge gaps on the biological implications of trypanosome co-infections in a single host, as well as the prevalence, vectors, life-cycle, host-range and clinical impact of most bat trypanosomes recorded to date. Continuous research efforts involving molecular surveillance of bat trypanosomes are required for improved disease prevention and control, mitigation of biosecurity risks and potential spill-over events, ultimately ensuring the health of humans, domestic animals and wildlife globally.