The potent greenhouse gas methane (CH4) is produced in the rumens of ruminant animals from hydrogen produced during microbial degradation of ingested feed. The natural animal-to-animal variation in the amount of CH4 emitted and the heritability of this trait offer a means for reducing CH4 emissions by selecting low-CH4 emitting animals for breeding. We demonstrate that differences in rumen microbial community structure are linked to high and low CH4 emissions in sheep. Bacterial community structures in 236 rumen samples from 118 high- and low-CH4 emitting sheep formed gradual transitions between three ruminotypes. Two of these (Q and S) were linked to significantly lower CH4 yields (14.4 and 13.6 g CH4/kg dry matter intake [DMI], respectively) than the third type (H; 15.9 g CH4/kg DMI; p<0.001). Low-CH4 ruminotype Q was associated with a significantly lower ruminal acetate to propionate ratio (3.7±0.4) than S (4.4±0.7; p<0.001) and H (4.3±0.5; p<0.001), and harbored high relative abundances of the propionate-producing Quinella ovalis. Low-CH4 ruminotype S was characterized by lactate- and succinate-producing Fibrobacter spp., Kandleria vitulina, Olsenella spp., Prevotella bryantii, and Sharpea azabuensis. High-CH4 ruminotype H had higher relative abundances of species belonging to Ruminococcus, other Ruminococcaceae, Lachnospiraceae, Catabacteriaceae, Coprococcus, other Clostridiales, Prevotella, other Bacteroidales, and Alphaproteobacteria, many of which are known to form significant amounts of hydrogen. We hypothesize that lower CH4 yields are the result of bacterial communities that ferment ingested feed to relatively less hydrogen, which results in less CH4 being formed.