Microbial electrosynthesis is a renewable energy and chemical production platform that relies on microbial taxa to capture electrons from a cathode and fix carbon. Yet the metabolic capacity of multispecies microbial communities on electrosynthetic biocathodes remains unknown. We assembled 13 genomes from a high-performing electroacetogenic culture, and mapped their transcriptional activity from a range of conditions. This allowed us to create a metabolic model of the primary community members (Acetobacterium, Sulfurospirillum, and Desulfovibrio). Acetobacterium was the primary carbon fixer, and a keystone member of the community. Based on transcripts upregulated near the electrode surface, soluble hydrogenases and ferredoxins from Acetobacterium and hydrogenases, formate dehydrogenase, and cytochromes of Desulfovibrio were essential conduits for electron flow from the electrode into the electrosynthetic community. A nitrogenase gene cluster with an adjacent ferredoxin and one of two Rnf complexes within the genome of the Acetobacterium were also upregulated on the electrode. Nitrogenase is known to serve as a hydrogenase, thereby it would contribute to hydrogen production by the biocathode. Oxygenases of microaerobic members of the community throughout the cathode chamber, including Sulfurospirillum and Rhodobacteraceae, were expressed. While the reactors were maintained anaerobically, this gene expression would support anaerobic growth and thus electrosynthesis by scrubbing small amounts of O2 out of the reactor. These molecular discoveries and metabolic modeling now serve as a foundation for future examination and development of electrosynthetic microbial communities.