The cathode microbial community of a methanogenic bioelectrochemical system (BES) is key to the efficient conversion of carbon dioxide (CO2) to methane (CH4) with application to biogas upgrading. The objective of this study was to compare the performance and microbial community composition of a biocathode inoculated with a mixed methanogenic (MM) culture to a biocathode inoculated with an enriched hydrogenotrophic methanogenic (EHM) culture, developed from the MM culture following pre-enrichment with H2 and CO2 as the only externally supplied electron donor and carbon source, respectively. Using an adjacent Ag/AgCl reference electrode, biocathode potential was poised at -0.8 V (versus SHE) using a potentiostat, with the bioanode acting as the counter electrode. When normalized to cathode biofilm biomass, the methane production in the MM- and EHM-biocathode was 0.153 ± 0.010 and 0.586 ± 0.029 mmol CH4/mg biomass-day, respectively. This study showed that H2/CO2 pre-enriched inoculum enhanced biocathode CH4 production, although the archaeal communities in both biocathodes converged primarily (86-100%) on a phylotype closely related to Methanobrevibacter arboriphilus. The bacterial community of the MM-biocathode was similar to that of the MM inoculum but was enriched in Spirochaetes and other nonexoelectrogenic, fermentative Bacteria. In contrast, the EHM-biocathode bacterial community was enriched in Proteobacteria, exoelectrogens, and putative producers of electron shuttle mediators. Similar biomass levels were detected in the MM- and EHM-biocathodes. Thus, although the archaeal communities were similar in the two biocathodes, the difference in bacterial community composition was likely responsible for the 3.8-fold larger CH4 production rate observed in the EHM-biocathode. Roles for abundant OTUs identified in the biofilm and inoculum cultures were highlighted on the basis of previous reports.