Marine dinitrogen (N2)-fixing cyanobacteria have large impacts on global biogeochemistry as they fix carbon dioxide (CO2) and fertilize oligotrophic ocean waters with new nitrogen. Iron (Fe) and phosphorus (P) are the two most important limiting nutrients for marine biological N2 fixation, and their availabilities vary between major ocean basins and regions. A long-standing question concerns the ability of two globally dominant N2-fixing cyanobacteria, unicellular Crocosphaera and filamentous Trichodesmium, to maintain relatively high N2-fixation rates in these regimes where both Fe and P are typically scarce. We show that under P-deficient conditions, cultures of these two cyanobacteria are able to grow and fix N2 faster when Fe deficient than when Fe replete. In addition, growth affinities relative to P increase while minimum concentrations of P that support growth decrease at low Fe concentrations. In Crocosphaera, this effect is accompanied by a reduction in cell sizes and elemental quotas. Relatively high growth rates of these two biogeochemically critical cyanobacteria in low-P, low-Fe environments such as those that characterize much of the oligotrophic ocean challenge the common assumption that low Fe levels can have only negative effects on marine primary producers. The closely interdependent influence of Fe and P on N2-fixing cyanobacteria suggests that even subtle shifts in their supply ratio in the past, present and future oceans could have large consequences for global carbon and nitrogen cycles.