Latent replication-competent HIV-1 persists in individuals on long-term antiretroviral therapy (ART). We developed the Full-Length Individual Proviral Sequencing (FLIPS) assay to determine the distribution of latent replication-competent HIV-1 within memory CD4+ T cell subsets in six individuals on long-term ART. FLIPS is an efficient, high-throughput assay that amplifies and sequences near full-length (∼9 kb) HIV-1 proviral genomes and determines potential replication competency through genetic characterization. FLIPS provides a genome-scale perspective that addresses the limitations of other methods that also genetically characterize the latent reservoir. Using FLIPS, we identified 5% of proviruses as intact and potentially replication competent. Intact proviruses were unequally distributed between T cell subsets, with effector memory cells containing the largest proportion of genetically intact HIV-1 proviruses. We identified multiple identical intact proviruses, suggesting a role for cellular proliferation in the maintenance of the latent HIV-1 reservoir. Display omitted •FLIPS utilizes NGS to sequence and genetically characterize HIV-1 proviruses•FLIPS identifies genetically intact and likely replication-competent HIV-1 proviruses•Identical HIV-1 proviruses suggest maintenance of reservoir by cellular proliferation•Demonstrate the advantages of FLIPS over other common HIV-1 sequencing assays Latent, replication-competent HIV-1 proviruses pose a significant barrier to an HIV-1 cure. Hiener et al. present the Full-Length Individual Proviral Sequencing (FLIPS) assay to reveal the distribution of genetically intact and potentially replication-competent HIV-1 proviruses in different T cell subsets isolated from individuals on long-term antiretroviral therapy.