We have discovered a new genus of endogenous Caulimoviridae, for which we propose the name Florendovirus, and found that endogenous florendoviral elements (EFEs) are common in most flowering plants including members of the Monocotyledoneae, the Eudicotyledonae and the so-called ANITA grade angiosperms. The identification of EFEs in Amborella trichopoda, an ancient endemic species of New Caledonia, suggests a minimum age of 85 million years for the florendoviruses based on the timing of separation of this Pacific island from the Australian landmass. In Ricinus communis, Jatropha curcas, Vitis vinifera and Citrus clementina, EFEs constitute more than 0.5% of the total nuclear genome content, which is a level of abundance that is comparable to that of high copy number transposable elements. In V. vinifera, c. 9% of the EFEs are located within host gene introns and when combined with the detection of EFE-derived small RNAs, suggests a role in plant metabolism by modifying gene expression. Molecular evidence suggests that some EFEs could be replication competent and potentially infectious. By analyzing reconstructed florendovirus genomes, we demonstrate that the florendoviruses are most closely related to but distinct from Petunia vein clearing virus based on the presence of a second open reading frame. Some of the ancestral viruses appeared to have had a bipartite genome organization, a feature that has never been observed before for any viral retroelement and that provides insights into the evolution of the Caulimoviridae.