Thaumarchaea, which represent as much as 20% of prokaryotic biomass in the open ocean, have been linked to environmentally relevant biogeochemical processes, such as ammonia oxidation (nitrification) and inorganic carbon fixation. We have used culture-independent methods to study this group because current cultivation limitations have proved a hindrance in studying these organisms. From a metagenomic data set obtained from surface waters from the Gulf of Maine, we have identified 36 111 sequence reads (containing 30 Mbp) likely derived from environmental planktonic Thaumarchaea. Metabolic analysis of the raw sequences and assemblies identified copies of the catalytic subunit required in aerobic ammonia oxidation. In addition, genes that comprise a nearly complete carbon assimilation pathway in the form of the 3-hyroxypropionate/4-hydroxybutyrate cycle were identified. Comparative genomics contrasting the putative environmental thaumarchaeal sequences and ‘Candidatus Nitrosopumilus maritimus SCM1’ revealed a number of genomic islands absent in the Gulf of Maine population. Analysis of these genomic islands revealed an integrase-associated island also found in distantly related microbial species, variations in the abundance of genes predicted to be important in thaumarchaeal respiratory chain, and the absence of a high-affinity phosphate uptake operon. Analysis of the underlying sequence diversity suggests the presence of at least two dominant environmental populations. Attempts to assemble complete environmental genomes were unsuccessful, but analysis of scaffolds revealed two diverging populations, including a thaumarchaeal-related scaffold with the full urease operon. Ultimately, the analysis revealed a number of insights into the metabolic potential of a predominantly uncultivated lineage of organisms. The predicted functions in the thaumarchaeal metagenomic sequences are directly supported by historic measurements of nutrient concentrations and provide new avenues of research in regards to understanding the role Thaumarchaea play in the environment.