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Anelloviruses are a ubiquitous component of healthy human viromes and remain highly prevalent after being acquired early in life. The full extent of "anellome" diversity and its evolutionary dynamics remain unexplored. We employed in-depth sequencing of blood-transfusion donor(s)-recipient pairs coupled with public genomic resources for a large-scale assembly of anellovirus genomes and used the data to characterize global and personal anellovirus diversity through time. The breadth of the anellome is much greater than previously appreciated, and individuals harbor unique anellomes and transmit lineages that can persist for several months within a diverse milieu of endemic host lineages. Anellovirus sequence diversity is shaped by extensive recombination at all levels of divergence, hindering traditional phylogenetic analyses. Our findings illuminate the transmission dynamics and vast diversity of anelloviruses and set the foundation for future studies to characterize their biology. [Display omitted] • Anellovirus genomes assembled from longitudinal blood-transfusion cohorts • Co-infections are common, with a median of six anellovirus lineages per subject • Transmitted anellovirus lineages were observed up to 260 days post-transfusion • Recombination is a key driver in anellovirus genomic diversification Anelloviruses comprise a major component of the healthy human virome. Arze et al. describe the extensive diversity of anellovirus genomes (the "anellome") in the blood of transfusion donors and recipients and uncover the dynamics of anellovirus transmission and persistence over several months after transfusion. [ABSTRACT FROM AUTHOR]