The anaerobic digestion of wastes is globally important in the production of methane (CH4) as a biofuel. When sulfate is present, sulfate-reducing bacteria (SRB) are stimulated, competing with methanogens for common substrates, which decreases CH4 production and results in the formation of corrosive, odorous hydrogen sulfide gas (H2S). Here, we show that a population of SRB within a methanogenic bioreactor fed only butyrate for years immediately (within hours) responded to sulfate availability and shifted the microbial community dynamics within the bioreactor. By mapping shotgun metatranscriptomes to metagenome-assembled genomes, we shed light on the transcriptomic responses of key community members in response to increased sulfate provision. We link these short-term transcriptional responses to long-term niche partitioning using comparative metagenomic analyses. Our results suggest that sulfate provision supports a syntrophic butyrate oxidation community that disfavors poly-beta-hydroxyalkanoate storage and that hydrogenotrophic SRB populations effectively exclude obligately hydrogenotrophic, but not aceticlastic, methanogens when sulfate is readily available. These findings elucidate key ecological dynamics between SRB, methanogens and syntrophic butyrate-oxidizing bacteria, which can be applied to a variety of engineered and natural systems.