Adaptive immunity requires the expansion of high affinity lymphocytes from a heterogenous pool. While current models explain this through signal transduction, we hypothesized that antigen affinity tunes discrete metabolic pathways to license clonal lymphocyte dynamics. Herein we identify NAD biosynthesis as a biochemical hub for the TCR affinity-dependent metabolome. Through its’ central anabolic role, NAD biosynthesis governs a quiescence exit checkpoint, pacing proliferation. Normalizing cellular NAD(H) likewise normalizes proliferation across affinities and enhancing NAD biosynthesis permits expansion of lower affinity clones. Furthermore, single-cell differences in NAD(H) predict division potential for both T- and B-cells, prior to the first division, unmixing proliferative heterogeneity. We believe this supports a broader paradigm in which complex signaling networks converge on metabolic pathways to control single-cell behavior.