The fate of diazotroph (N2 fixers) derived carbon (C) and nitrogen (N) and their contribution to vertical export of C and N in the Western Tropical South Pacific Ocean was studied in OUTPACE (Oligotrophy to UlTra-oligotrophy PACific Experiment). Our specific objective during OUTPACE was to determine whether autocatalytic programmed cell death (PCD) is an important mechanism affecting diazotroph mortality and a factor regulating the vertical flux of organic matter and thus the fate of the blooms. We sampled at three long duration (LD) stations of 5 days each (LDA, LDB, and LDC) where drifting sediment traps were deployed at 150, 325 and 500 m depths. LDA and LDB were characterized by high chlorophyll a (Chl a) concentrations (0.2–0.6 µg L−1) and dominated by dense biomass of Trichodesmium as well as UCYN-B and diatom-diazotroph associations (Rhizosolenia with Richelia-detected by microscopy and het-1 nifH copies). Station LDC was located at an ultra-oligotrophic area of the South Pacific gyre with extremely low Chl a concentration (~ 0.02 µg L−1) with limited biomass of diazotrophs predominantly the unicellular UCYN-B. Our measurements of biomass from LDA and LDB yielded high activities of caspase-like and metacaspase proteases that are indicative of PCD in Trichodesmium and other phytoplankton. Metacaspase activity, reported here for the first time from oceanic populations, was highest at the surface of both LDA and LDB, where we also obtained high concentrations of transparent exopolymeric particles (TEP). TEP was negatively correlated with dissolved inorganic phosphorus and positively coupled to both the DOC and POC pools reflecting the typically high production of TEP under nutrient stress and its role as a source of sticky carbon facilitating aggregation and rapid vertical sinking. Evidence for bloom decline was observed at both LDA and LDB. However, the physiological status and rates of decline of the blooms differed between the stations, influencing the amount of accumulated diazotrophic organic matter and mass flux observed in the traps during our experimental time frame. At LDA sediment traps contained the greatest export of particulate matter and significant numbers of both intact and decaying Trichodesmium, UCYN-B, and het-1 compared to LDB where the bloom decline began only 2 days prior to leaving the station and to LDC where no evidence for bloom decline was seen. Substantiating previous findings from laboratory cultures linking PCD to carbon export in Trichodesmium, our results from OUTPACE indicate that induction of PCD by nutrient limitation in high biomass blooms such as Trichodesmium or diatom-diazotroph associations combined with high TEP production facilitates cellular aggregation and bloom termination, and expedites vertical flux to depth