The viromes of land plants are enormous and diverse, and they are dominated by RNA viruses. However, reverse-transcription and single-stranded (ss) DNA viruses also make significant contributions to the viromes of land plants. In this article, we present a thorough taxonomy of viruses that was recently adopted and is based on phylogenomic investigations. This taxonomy is then applied to the plant virome. We continue our investigation by tracing the evolutionary origins of various plant virus lineages all the way back to the first genetic mobile components. We investigate the role of horizontal viral transfer from invertebrates to plants during terrestrialization, which was enabled by strong ecological linkages. The intimate evolution of invertebrates and plants permitted these relationships. We hope that plant biologists and virologists will be interested in the evolving big picture of the plant virome’s origins and global architecture, which will encourage further research into virus–plant coevolution.