The controls on the ‘Redfield’ N : P stoichiometry of marine phytoplankton and hence the N : P ratio of the deep ocean remain incompletely understood. Here, we use a model for phytoplankton ecophysiology and growth, based on functional traits and resource-allocation trade-offs, to show how environmental filtering, biotic interactions, and element cycling in a global ecosystem model determine phytoplankton biogeography, growth strategies and macromolecular composition. Emergent growth strategies capture major observed patterns in marine biomes. Using a new synthesis of experimental RNA and protein measurements to constrain per-ribosome translation rates, we determine a spatially variable lower limit on adaptive rRNA:protein allocation and hence on the relationship between the largest cellular P and N pools. Comparison with the lowest observed phytoplankton N : P ratios and N : P export fluxes in the Southern Ocean suggests that additional contributions from phospholipid and phosphorus storage compounds play a fundamental role in determining the marine biogeochemical cycling of these elements.