The processes that underpin maintenance of human NK cells remain unclear, with growing evidence for homeostatic mechanisms beyond continual supply by haematopoietic precursors. Here, we developed a novel flow cytometry assay to explore the role of self-renewing proliferation in maintaining the peripheral blood NK cell pool. Our assay uses a combination of antibodies to delineate cell-cycle states in unmanipulated ex vivo samples. Examining freshly isolated human PBMCs, we observed actively cycling cells (in S or G2/M phase) across the NK cell pool. Frequencies of actively cycling cells were similar between CD56^bright and conventional CD56^dim NK cells, spanning maturation and HLA-education status. In contrast, significantly less proliferation of expanded adaptive NK cells was seen in cytomegalovirus-infected individuals. In general, for conventional NK cells, the phenotype of cycling cells largely reflected the individual donor’s subset distribution, indicating self-renewal across the NK cell pool at steady state. While the frequency of actively cycling NK cells was mostly uniform across subsets, the CD56^bright population was highly enriched for cells that had recently exited cell cycle. This paralleled extensive cycling of tonsil-tissue CD56^bright NK cells and precursors, relative to CD56^dim NK cells. In understanding the drivers of NK cell proliferation in peripheral blood, we observed transiently upregulated CD56 expression, suggestive of recent IL-15 exposure. Elevated pSTAT5 and downstream IL-15 signalling molecules detected ex vivo by flow cytometry and single-cell RNA sequencing further supported a role for IL-15 in driving proliferation. To assess turnover in peripheral blood we combined our cell cycle markers with apoptosis detection by flow cytometry. Actively cycling NK cells exhibited significantly higher apoptosis rates compared to quiescent or recently divided NK cells. Together, we provide evidence for self-renewing turnover in the periphery of mature human NK cells across the conventional and adaptive NK cell compartments.