The oceanic crust forms two thirds of the Earth’s surface and hosts a large phylogenetic and functional diversity of microorganisms. While advances have been made in the sedimentary realm, our understanding of the igneous rock portion as a microbial habitat has remained limited. We present the first comparative metagenomic microbial community analysis from ocean floor basalt environments at the Lō’ihi Seamount, Hawai’i, and the East Pacific Rise (EPR; 9°N). Phylogenetic analysis indicates the presence of a total of 43 bacterial and archaeal mono-phyletic groups, dominated by Alpha- and Gammaproteobacteria, as well as Thaumarchaeota. Functional gene analysis suggests that these Thaumarchaeota play an important role in ammonium oxidation on seafloor basalts. In addition to ammonium oxidation, the seafloor basalt habitat reveals a wide spectrum of other metabolic potentials, including CO2 fixation, denitrification, dissimilatory sulfate reduction, and sulfur oxidation. Basalt communities from Lō’ihi and the EPR show considerable metabolic and phylogenetic overlap down to the genus level despite geographic distance and slightly different seafloor basalt mineralogy.