Microbial electrosynthesis is the conversion of CO2­ to chemicals by autotrophic microorganisms using reducing equivalents from a negatively poised electrode. The technology is in the nascent stage of development, but has the potential to be a sustainable, carbon-consuming platform for industrial chemical and fuel production. To date, microbial electrosynthesis of acetate, the first step in order to generate liquid fuels from CO2, has been characterized by low rates and yields. In order for microbial electrosynthesis systems to become commercially relevant, long- term operation and improved rates must be demonstrated. To address these issues, bioelectrochemical reactors were operated chronoamperometrically at a cathode potential of -590 mV vs. SHE for over 200 days. Hydrogen, acetate, and methane were produced by adaptively evolved microbiomes at rates 10-100x what has been previously reported. Other products observed were formate, propionate, and butyrate. Acetobacterium spp. dominated the active microbial population on the cathodes (50-60%), with members of Sulfurospirillum and the Rhodobacteraceae also prevalent. Further experimental results demonstrate stability, resilience, and improved performance of electrosynthetic biocathodes following long-term operation. Sustained product formation at faster rates by a carbon-capturing microbiome is a key milestone addressed in this work that advances microbial electrosynthesis systems towards commercialization.