AbstractN₂ fixation constitutes an important new nitrogen source in the open sea. One group of filamentous N₂ fixing cyanobacteria (Richelia intracellularis, hereafter Richelia) form symbiosis with a few genera of diatoms. High rates of N₂ fixation and carbon (C) fixation have been measured in the presence of diatom-Richelia symbioses. However, it is unknown how partners coordinate C fixation and how the symbiont sustains high rates of N₂ fixation. Here, both the N₂ and C fixation in wild diatom-Richelia populations are reported. Inhibitor experiments designed to inhibit host photosynthesis, resulted in lower estimated growth and depressed C and N₂ fixation, suggesting that despite the symbionts ability to fix their own C, they must still rely on their respective hosts for C. Single cell analysis indicated that up to 22% of assimilated C in the symbiont is derived from the host, whereas 78–91% of the host N is supplied from their symbionts. A size-dependent relationship is identified where larger cells have higher N₂ and C fixation, and only N₂ fixation was light dependent. Using the single cell measures, the N-rich phycosphere surrounding these symbioses was estimated and contributes directly and rapidly to the surface ocean rather than the mesopelagic, even at high estimated sinking velocities (<10 m d⁻¹). Several eco-physiological parameters necessary for incorporating symbiotic N₂ fixing populations into larger basin scale biogeochemical models (i.e., N and C cycles) are provided.