The diversity, origin, and evolution of chromoviruses in Eukaryota were examined using the massive amount of genome sequence data for different eukaryotic lineages. A surprisingly large number of novel full-length chromoviral elements were found, greatly exceeding the number of the known chromoviruses. These new elements are mostly structurally intact and highly conserved. Chromoviruses in the key Amniota lineage, the reptiles, have been analyzed by PCR to explain their evolutionary dynamics in amniotes. Phylogenetic analyses provide evidence for a novel centromere-specific chromoviral clade that is widespread and highly conserved in all seed plants. Chromoviral diversity in plants, fungi, and vertebrates, as shown by phylogenetic analyses, was found to be much greater than previously expected. The age of plant chromoviruses has been significantly extended by finding their representatives in the most basal plant lineages, the green and the red algae. The evolutionary origin of chromoviruses has been found to be no earlier than in Cercozoa. The evolutionary history and dynamics of chromoviruses can be explained simply by strict vertical transmission in plants, followed by more complex evolution in fungi and in Metazoa. The currently available data clearly show that chromoviruses indeed represent the oldest and the most widespread clade of Metaviridae.