Differences in relative availability of nitrate vs. phosphate may contribute to regional variations in plankton elemental stoichiometry. As a representative of the globally abundant marine Synechococcus, strain WH8102 was grown in 16 chemostats up to 52 d at a fixed growth rate with nitrogen–phosphorus ratios (N : Psupply) of 1–50. Initially, the phosphate and nitrate concentrations in the vessel decreased when the respective nutrient was limiting. Cell growth generally stabilized, although several chemostats had apparent oscillations in biomass. We observed extensive plasticity in the elemental content and ratios. N : Pcell matched the supply values between N : Psupply 5 and 20. The C : Pcell followed a similar trend. In contrast, the mean C : Ncell was 6.8 and did not vary as a function of supply ratios. We also observed that induction of alkaline phosphatase, the fraction of P allocated to nucleic acids, and the lipid sulfoquinovosyldiacylglycerol : phosphatidyglycerol ratio inversely correlated with P availability. Our results suggest that this extensive plasticity in the elemental content and ratios depends both on the external nutrient availability as well as past growth history. Thus, our study provides a quantitative understanding of the regulation of the elemental stoichiometry of an abundant ocean phytoplankton lineage.