Marine regions that experience low dissolved oxygen (DO) from seasonal to long-term time scales, a.k.a. dead zones, are increasing in number and severity around the globe with deleterious effects on ecology and economics. One of the largest of these occurs on the continental shelf of the northern Gulf of Mexico (nGOM) as a result of eutrophication-enhanced bacterioplankton respiration and strong stratification. The effects of this perturbation on microbial assemblages, and therefore the underlying potential for biogeochemical cycling, have only begun to be explored. Here we present predicted roles for multiple organisms in various phases of nitrogen, carbon, and sulfur cycling and evidence for electron donor-based niche partitioning based on more than 70 high-quality genomes (33 of which are > 70% complete) reconstructed from whole community metagenomic data in the 2013 nGOM dead zone and metatranscriptomic expression data. All but two genomes could be classified into 17 named bacterial and archaeal phyla, and many represented the most abundant organisms in the dead zone (e.g. Thaumarchaeota, Synechococcus), some of which include members of the uncultivated microbial dark matter (e.g. Marine group II Euryarchaeota, SAR406). Surprisingly, we also recovered near complete genomes belonging to Candidate Phyla that are usually associated with anoxic environments: Parcubacteria (OD1), Peregrinibacteria, Latescibacteria (WS3), and ACD39. This work provides an important biogeochemical map for multiple phyla that will help to resolve the impacts of hypoxia on nutrient flow in the dead zone.