Bats, rodents, and shrews are the most important animal sources of human infectious diseases. However, the evolution and transmission of viruses among them remain largely unexplored. Through the meta-transcriptomic sequencing of internal organ and fecal samples from 2,443 wild bats, rodents, and shrews sampled from four Chinese habitats, we identified 669 viruses, including 534 novel viruses, thereby greatly expanding the mammalian virome. Our analysis revealed high levels of phylogenetic diversity, identified cross-species virus transmission events, elucidated virus origins, and identified cases of invertebrate viruses in mammalian hosts. Host order and sample size were the most important factors impacting virome composition and patterns of virus spillover. Shrews harbored a high richness of viruses, including many invertebrate-associated viruses with multi-organ distributions, whereas rodents carried viruses with a greater capacity for host jumping. These data highlight the remarkable diversity of mammalian viruses in local habitats and their ability to emerge in new hosts. Display omitted •A large number of novel viruses were identified in wild small mammals from China•Some were of evolutionary significance or had the ability to jump species boundaries•Shrews carried the most viruses in total and in a single animal species•Rodents harbored most viruses with the potential be transmitted to new host species A large study of the mammalian virome identifies differences across rodents, bats, and shrews, revealing insights into host range, transmission, and potential pathogens with the ability to jump across species.