Adult T cell leukemia/lymphoma (ATL) occurs in ~5% of HTLV-1-infected individuals and is conventionally thought to be a monoclonal disease, in which a single HTLV-1(+) T cell clone progressively outcompetes others and undergoes malignant transformation. Here, using a sensitive high-throughput method we quantified clonality in 197 ATL cases, identified genomic characteristics of the proviral integration sites in malignant and non-malignant clones, and investigated the proviral features (genomic structure and 5'LTR methylation) that determine its capacity to express the HTLV-1 oncoprotein Tax. Of the dominant, presumed malignant clones, 91% contained a single provirus. The genomic characteristics of the integration sites in the ATL clones resembled those of the frequent low-abundance clones (present in both ATL cases and carriers) and not those of the intermediate-abundance clones observed in 24% of ATL cases, suggesting that oligoclonal proliferation per se does not cause malignant transformation. Gene ontology analysis revealed an association in 6% of cases between ATL and integration near host genes in 3 functional categories, including genes previously implicated in haematological malignancies. In all cases of HTLV-1 infection, regardless of ATL, there was evidence of preferential survival of the provirus in vivo in acrocentric chromosomes (13, 14, 15, 21 and 22).