Land plants host a vast and diverse virome that is dominated by RNA viruses, with major additional contributions from reverse-transcribing and single-stranded (ss) DNA viruses. Here, we introduce the recently adopted comprehensive taxonomy of viruses based on phylogenomic analyses, as applied to the plant virome. We further trace the evolutionary ancestry of distinct plant virus lineages to primordial genetic mobile elements. We discuss the growing evidence of the pivotal role of horizontal virus transfer from invertebrates to plants during the terrestrialization of these organisms, which was enabled by the evolution of close ecological associations between these diverse organisms. It is our hope that the emerging big picture of the formation and global architecture of the plant virome will be of broad interest to plant biologists and virologists alike and will stimulate ever deeper inquiry into the fascinating field of virus–plant coevolution.

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