The microbially mediated anaerobic oxidation of methane (AOM) is critical for regulating the flux of methane from the ocean and is coupled to sulfate reduction (SR) in many anoxic marine environments. Sulfate-dependent AOM is performed by specialized groups of anaerobic methane-oxidizing (ANME) archaea, which are thought to form consortial relationships with sulfate-reducing bacteria (SRB). Certain ANME and SRB groups have been shown to occupy different ecological niches in hydrocarbon-rich deep sea sediments. However, the environmental parameters that select for certain phylogenetic variants are still unknown. In this study, we generated the largest dataset to date of 16S rRNA gene sequences for these uncultivable microorganisms to gain a better understanding of the distribution of these methane- and sulfur- cycling ecotypes in biogeochemically distinct deep sea sediment ecosystems. Sediment strata were collected from the cold seeps of Hydrate Ridge, metalliferous sedimented hydrothermal vents of Juan de Fuca Ridge, and organic-rich hydrothermally influenced sediments of Guaymas Basin. In this comparative study, we used the Illumina MiSeq sequencing platform to assess archaeal and bacterial richness, diversity, and taxonomic composition followed by phylogenetic analyses of ANME and SRB phylotypes. Environmental data were used to establish the relationships between ANME and SRB phylotype distribution and environmental gradients as well as the extent of these functional groups in different hydrocarbon-rich ecosystems. Our results indicate that physicochemical constraints, particularly temperature and substrate availability, drive the distribution of different ANME and SRB ecotypes and the associated communities in spatially separated sites.