In the open ocean, elevated carbon flux (ECF) events increase the delivery of particulate carbon from surface waters to the seafloor by severalfold compared to other times of year. Since microbes play central roles in primary production and sinking particle formation, they contribute greatly to carbon export to the deep sea. Few studies, however, have quantitatively linked ECF events with the specific microbial assemblages that drive them. Here, we identify key microbial taxa and functional traits on deep-sea sinking particles that correlate positively with ECF events. Microbes enriched on sinking particles in summer ECF events included symbiotic and free-living diazotrophic cyanobacteria, rhizosolenid diatoms, phototrophic and heterotrophic protists, and photoheterotrophic and copiotrophic bacteria. Particle-attached bacteria reaching the abyss during summer ECF events encoded metabolic pathways reflecting their surface water origins, including oxygenic and aerobic anoxygenic photosynthesis, nitrogen fixation, and proteorhodopsin-based photoheterotrophy. The abundances of some deep-sea bacteria also correlated positively with summer ECF events, suggesting rapid bathypelagic responses to elevated organic matter inputs. Biota enriched on sinking particles during a spring ECF event were distinct from those found in summer, and included rhizaria, copepods, fungi, and different bacterial taxa. At other times over our 3-y study, mid- and deep-water particle colonization, predation, degradation, and repackaging (by deep-sea bacteria, protists, and animals) appeared to shape the biotic composition of particles reaching the abyss. Our analyses reveal key microbial players and biological processes involved in particle formation, rapid export, and consumption, that may influence the ocean’s biological pump and help sustain deep-sea ecosystems.