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Rich geochemical datasets generated over the past 30 years have provided fine-scale resolution on the northern Gulf of Mexico (nGOM) coastal hypoxic (<= 2 mg of O-2 L-1) zone. In contrast, little is known about microbial community structure and activity in the hypoxic zone despite the implication that microbial respiration is responsible for forming low dissolved oxygen (DO) conditions. Here, we hypothesized that the extent of the hypoxic zone is a driver in determining microbial community structure, and in particular, the abundance of ammonia-oxidizing archaea (AOA). Samples collected across the shelf for two consecutive hypoxic seasons in July 2013 and 2014 were analyzed using 16S rRNA gene sequencing, oligotyping, microbial co-occurrence analysis, and quantification of thaumarchaeal 16S rRNA and archaeal ammonia-monooxygenase (amoA) genes. In 2014 Thaumarchaeota were enriched and inversely correlated with DO while Cyanobacteria, Acidimicrobiia, and Proteobacteria where more abundant in oxic samples compared to hypoxic. Oligotyping analysis of Nitrosopumilus 16S rRNA gene sequences revealed that one oligotype was significantly inversely correlated with DO in both years. Oligotyping analysis revealed single nucleotide variation among all Nitrosopumilaceae, including Nitrosopumilus 16S rRNA gene sequences, with one oligotype possibly being better adapted to hypoxia. We further provide evidence that in the hypoxic zone of both year 2013 and 2014, low DO concentrations and high Thaumarchaeota abundances influenced microbial co-occurrence patterns. Taken together, the data demonstrated that the extent of hypoxic conditions could potentially drive patterns in microbial community structure, with two years of data revealing the annual nGOM hypoxic zone to be emerging as a low DO adapted AOA hotspot.