Bats host many viruses pathogenic to humans, and increasing evidence suggests that Rotavirus A (RVA) also belongs to this list. Rotaviruses cause diarrheal disease in many mammals and birds, and their segmented genomes allow them to reassort and increase their genetic diversity. Eighteen out of 2,142 bat faecal samples (0.8%) collected from Europe, South America and Africa were PCR-positive for RVA and 11 of those were fully characterized using viral metagenomics. Upon contrasting their genomes with publicly available data, at least 7 distinct bat RVA genotype constellations were identified, including evidence of reassortments among them. Some of these constellations are spread across the world, whereas others appear to be geographically restricted. Our analyses also provide evidence for multiple zoonotic transfer events involving bat RVAs. A Bulgarian bat RVAs possessed a genotype constellation previously identified in Chinese bats, and identical to a rare Argentinean horse RVA. A Costa Rican bat RVA possessed 3 previously undescribed gene segments and clustered closely with a human strain. Although SA11 is one of the most widely used reference strains for RVA research and forms the backbone of a reverse genetics system, its origin remained enigmatic. Remarkably, the majority of the gene segments of SA11 were closely related to Gabonese bat RVAs, suggesting a potential bat origin. Overall, our findings suggest an underexplored genetic diversity of RVAs in bats which is likely the tip of the iceberg. Increasing contact between humans and bat wildlife will further increase the zoonosis risk, which warrants closer attention to these viruses. ImportanceThe increased research on bat coronaviruses after SARS-CoV and MERS-CoV, allowed the very rapid identification of SARS-CoV-2. This is an excellent example of the importance of knowing viruses harboured by wildlife in general and bats in particular, for global preparedness against emerging viral pathogens. The current effort to characterise bat rotavirus strains from 3 continents provided evidence that several atypical rotaviruses in humans and animals might have a bat origin, implying that zoonoses of bat rotaviruses occur more frequently than currently realized.