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The photosynthetic cyanobacterium Trichodesmiumis widely distributed in the surface low latitude ocean where it contributes significantly to N2fixation and primary productivity. Previous studies found nifHgenes and intact Trichodesmiumcolonies in the sunlight-deprived meso- and bathypelagic layers of the ocean (200–4000?m depth). Yet, the ability of Trichodesmiumto fix N2in the dark ocean has not been explored. We performed 15N2incubations in sediment traps at 170, 270 and 1000?m at two locations in the South Pacific. Sinking Trichodesmiumcolonies fixed N2at similar rates than previously observed in the surface ocean (36–214?fmol N cell-1d-1). This activity accounted for 40?±?28% of the bulk N2fixation rates measured in the traps, indicating that other diazotrophs were also active in the mesopelagic zone. Accordingly, cDNA nifHamplicon sequencing revealed that while Trichodesmiumaccounted for most of the expressed nifHgenes in the traps, other diazotrophs such as Chlorobiumand Deltaproteobacteria were also active. Laboratory experiments simulating mesopelagic conditions confirmed that increasing hydrostatic pressure and decreasing temperature reduced but did not completely inhibit N2fixation in Trichodesmium. Finally, using a cell metabolism model we predict that Trichodesmiumuses photosynthesis-derived stored carbon to sustain N2fixation while sinking into the mesopelagic. We conclude that sinking Trichodesmiumprovides ammonium, dissolved organic matter and biomass to mesopelagic prokaryotes.