Determining the role of rumen microbes in plant polysaccharide breakdown is fundamental to understanding digestion, and maximising productivity, in ruminant animals. Rumen bacterial species belonging to the genera Butyrivibrio and Pseudobutyrivibrio are important degraders of plant hemicelluloses, abundant heterogeneous, branched polymers involved in crosslinking cellulose microfibrils to lignin. To investigate the core genes required for their hemicellulose-degrading lifestyle in the rumen, the genomes of 39 Butyrivibrio and 6 Pseudobutyrivibrio strains, isolated from the plant-adherent microbiome of New Zealand bovine ruminants, have been sequenced. To examine differences between the hemicellulose-degrading functions of Butyrivibrio and Pseudobutyrivibrio species, their CAZyme-encoding genes were compared. Within the Butyrivibrio and Pseudobutyrivibrio pan-genomes, respectively, there were a total of 3586 and 293 glycoside hydrolases, 249 and 16 carbohydrate esterases. To examine species differences, the genes of the previously characterised bacterium B. proteoclasticus B316 were compared in detail with those from the newly sequenced B. hungatei MB2003. B316 was found to encode a much more developed polysaccharide-degrading repertoire and we hypothesised that B316 would out-compete MB2003 when grown in co-culture on the insoluble hemicellulose substrate, xylan. To test this hypothesis, the two strains were grown on xylan, either alone in monocultures, or in direct competition in a co-culture. The results showed that MB2003 had little ability to utilise xylan alone, but was capable of significant growth when co-cultured with B316. This indicates a commensalistic interaction between these species, in which B316 initiates the primary attack on the insoluble substrate, while MB2003 has a secondary role, competing for the released soluble sugars. This work provides the first systematic phenotypic, comparative genomic and functional analysis of ruminal Butyrivibrio and Pseudobutyrivibrio species, which not only defines their conserved features involved in hemicellulose degradation, but is also beginning to differentiate their unique gene complements and growth characteristics that separate them as discrete species.