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Mammalian genomes typically contain hundreds of thousands of endogenous retroviruses (ERVs), derived from ancient retroviral infections. Using this molecular 'fossil' record, we reconstructed the natural history of a specific retrovirus lineage (ERV-Fc) that disseminated widely between ~33 and ~15 million years ago, corresponding to the Oligocene and early Miocene epochs. Intercontinental viral spread, numerous instances of interspecies transmission and emergence in hosts representing at least 11 mammalian orders, and a significant role for recombination in diversification of this viral lineage were also revealed. By reconstructing the canonical retroviral genes, we identified patterns of adaptation consistent with selection to maintain essential viral protein functions. Our results demonstrate the unique potential of the ERV fossil record for studying the processes of viral spread and emergence as they play out across macro-evolutionary timescales, such that looking back in time may prove insightful for predicting the long-term consequences of newly emerging viral infections. DOI: http://dx.doi.org/10.7554/eLife.12704.001, eLife digest Viruses have been with us for billions of years, and exist everywhere in nature that life is found. Viruses therefore have had a significant impact on the evolution of all organisms, from bacteria to humans. Unfortunately, viruses do not leave fossils, and so we know very little about how viruses originate and evolve over time. Fortunately, over the course of millions of years, genetic sequences from the viruses accumulate in the DNA genomes of living organisms (including humans). These sequences can serve as molecular “fossils” for exploring the natural history of viruses and their hosts. Diehl et al. have now searched the genomes of 50 modern mammals for “fossil” viral remnants of an ancient group of viruses known as ERV-Fc. This revealed that ERV-Fc viruses infected the ancestors of at least 28 of these mammal species between 15 million and 30 million years ago. The viruses affected a diverse range of hosts, including carnivores, rodents and primates. The distribution of ERV-Fc among different mammals indicates that the viruses spread to every continent except Antarctica and Australia, and that they jumped between species more than 20 times. Diehl et al. also pinpointed patterns of evolutionary change in the genes of the ERV-Fc viruses that reflect how the viruses adapted to different host mammals. As part of this process, the viruses often exchanged genes with each other and with other types of viruses. Such genetic recombination is likely to have played a significant role in the evolutionary success of the ERV-Fc viruses. Mammalian genomes contain hundreds of thousands of ancient viral fossils similar to ERV-Fc. Future work could study these to improve our understanding of when and why new viruses emerge and how long-term contact with viruses affects the evolution of their host organisms. DOI: http://dx.doi.org/10.7554/eLife.12704.002