Protozoa comprise a major fraction of the microbial biomass in the rumen microbiome, of which the genus Entodinium has been consistently observed to be dominant across a diverse genetic and geographical range of ruminant hosts. Despite the apparent core role that species such as Entodinium caudatum exert, their major biological and metabolic contributions to rumen function remain largely undescribed. Here, we have leveraged (meta)genome-centric metaproteomes from rumen fluid samples originating from both cattle and goats fed diets with varying inclusion levels of lipids and starch, to detail the specific metabolic niches that E. caudatum occupies in the context of its microbial co-habitants. Initial proteome estimations via total protein counts and label-free quantification highlight that E. caudatum comprises an extensive fraction of the total rumen metaproteome. Our analysis also suggested increased microbial predation and volatile fatty acid (VFA) metabolism by E. caudatum to occur in high methane-emitting animals, although with no apparent direct metabolic link to methanogenesis. Despite E. caudatum having a well-established reputation for digesting starch, it was unexpectedly less detectable in low methane emitting-animals fed high starch diets, which were instead dominated by propionate/succinate-producing bacterial populations suspected of being resistant to predation irrespective of host. Finally, we reaffirmed our abovementioned observations in geographically independent datasets, thus illuminating the substantial metabolic influence that under-explored eukaryotic populations have in the rumen, with greater implications for both digestion and methane metabolism.