Macroevolution describes the evolutionary processes occurring over time scales of major evolutionary events; for example, the emergence of the mammals. While the short-term processes of virus evolution are frequently studied, we know little about how viruses have evolved over the timescale of their hosts’ evolutionary history. Marsupials are one of the most basal lineages within the mammals and have a unique evolutionary history in that they first emerged in parts of the ancient supercontinent, Gondwana, in what is now the Americas and a subset of the population migrated to their present-day home in Australia where they diversified to fill a range of environmental niches. This presents a unique opportunity to study virus evolution within this distinct host lineage. Sampling Australian Marsupials using unbiased metagenomic virus discovery methods has unearthed a number of novel virus species including a novel henipavirus in Antechinus, the first marsupial associated delta-like viruses and a number of novel hepacivirus species. The identification of a highly divergent hepacivirus in Numbats and the first mammalian infecting species within the Jingchuvirales challenge our understanding of mammalian virus evolution and the host specificity of some viral taxa. Furthermore, this approach has revealed concerning host-jumping events from introduced eutherian species to endangered wildlife in Australia, highlighting the potential disease impacts of invasive species.