Oceanic oxygen deficient zones (ODZs) are globally significant sites of biogeochemical cycling where microorganisms deplete dissolved oxygen (DO) to anoxia. Amid intense competition for DO in these challenging environments, aerobic ammonia- and nitrite-oxidizing organisms are abundant and may consume significant amounts of DO—effectively engineering ODZs and unlocking anaerobic nitrogen (N) cycling processes such as denitrification. Despite their fundamental biogeochemical importance, how these processes and organisms compete, interact, and ultimately drive ODZ carbon, oxygen, and N cycling remains poorly understood. Using parallel measurements of DO consumption rates and 15N-based oxidation rates applied to both water column profiles and oxygen manipulation experiments, as well as 16S and metagenome sequencing, we show that the contribution of nitrite oxidation to overall DO consumption systematically increases as DO declines in the eastern tropical North Pacific (ETNP) ODZ. Nitrite oxidation could account for all DO consumption under DO concentrations <393 nM found in and below the secondary chlorophyll maximum. In contrast, ammonia oxidation was more sensitive to DO levels and occurred at slower but detectable rates. Although three groups of nitrite-oxidizing Nitrospina bacteria and three groups of ammonia-oxidizing archaea (AOA) were dominant in the ETNP, they displayed contrasting distributions throughout the ODZ water column: individual Nitrospina ecotypes were confined to specific biogeochemical niches, whereas AOA were not differentiated with depth. Metagenome-assembled genomes (MAGs) were assembled for all three AOA groups, including a new AOA MAG grouping that differed in genomic content from previously recovered MAGs. We further show that Nitrospina and AOA both respond to sharp shifts driven by a Category 4 hurricane sampled at sea. Phytoplankton blooming in the wake of the storm, combined with rapid and severe ODZ shoaling, fueled intense carbon and N cycling in a hurricane-driven ‘microbial bloom.’ Our combined results indicate that multiple groups of ammonia and nitrite oxidizers are finely tuned to ODZ environmental conditions, and so optimized to exploit and rapidly cycle scarce and transient biogeochemical resources.