The generation of T cell diversity is critical to an effective immune response, but the mechanism by which this diversity emerges is not fully understood. An appealing explanation is the control of T cell heterogeneity by differential exposure of individual cells to external signalling molecules. However, a high degree of population heterogeneity in both division progression and phenotype is preserved even in strongly controlled in vitro stimulatory conditions and in genetically uniform T cells, such as OT-I TCR transgenics. This suggests that cell intrinsic mechanisms make a substantial contribution to the generation of population-level phenotypic diversity, yet a precise characterisation of these mechanisms remains elusive. Previous studies of lymphocyte division kinetics have revealed that population heterogeneity is underpinned by clonal synchrony in division properties. To examine whether phenotypic heterogeneity is similarly regulated at the clonal level, we adapted a novel in vitro clonal lineage tracing technique using multiplexed division tracking dyes to characterise the clonal heritage, division progression and phenotype of CD8+ T cells shortly after activation. This enabled us to examine the relative contribution of intra- and inter-clonal variation to overall population diversity, revealing substantial intraclonal concordance and interclonal variability in cell surface marker expression. This provides evidence of a mechanism whereby heritable information is imprinted in naïve founder cells during activation, which is subsequently passed on to progeny cells undergoing clonal expansion.