Recent measurements of natural populations of the marine cyanobacterium Prochlorococcus indicate this numerically dominant phototroph assimilates phosphorus (P) at significant rates in P-limited oceanic regions. To better understand uptake capabilities of Prochlorococcus under different P stress conditions, uptake kinetic experiments were performed on ProchlorococcusMED4 grown in P-limited chemostats and batch cultures. Our results indicate that MED4 has a small cell-specific Vmax but a high specific affinity (αP) for P, making it competitive with other marine cyanobacteria at low P concentrations. Additionally, MED4 regulates its uptake kinetics in response to P stress by significantly increasing Vmax and αP for both inorganic and organic P (PO4 and ATP). The Michaelis-Menten constant, KM, for PO4 remained constant under different P stress conditions, whereas the KM for ATP was higher when cells were stressed for PO4, pointing to additional processes involved in uptake of ATP. MED4 cleaves the PO4 moieties from ATP, likely with a 5′-nucleotidase-like enzyme rather than alkaline phosphatase. MED4 exhibited distinct physiological differences between cells under steady-state P limitation versus those transitioning from P-replete to P-starved conditions. Thus, MED4 employs a variety of strategies to deal with changing P sources in the oceans and displays complexity in P stress acclimation and regulatory mechanisms.