Ruminants sustain a long-lasting obligatory relationship with their rumen microbiome dating back 50 million years. In this unique host-microbiome relationship the host’s ability to digest its feed is completely dependent on its coevolving microbiome. This extraordinary alliance raises questions regarding the dependence of ruminants’ genetics and physiology on the rumen microbiome structure, composition and metabolisem. To elucidate this relationship we examined association of host genetics to phylogenetics and functional composition of the rumen microbiome. We accomplished this using a 50K bovine genome single nucleotide polymorphism chip over a set of 47 animals that was used to identify microbial Operational Taxonomic Units (OTUs) associated with host genetics. Heritable bovine rumen OTUs were in turn tested for association with rumen metabolites and host related characteristics along a cohort of 78 milking Holstein-Friesian cows, including the genotyped cows. We found 22 bacterial OTUs whose abundances were found to be associated with animal genetics, rumen metabolism and host physiology. The abundance patterns of these microbes can explain high proportions of variance in rumen metabolism and many of the host physiological attributes such as its energy harvest efficiency. Interestingly, these OTUs shared higher phylogenetic similarity between themselves than expected by chance, suggesting occupation of a specific ecological niche within the rumen ecosystem. The findings presented herein suggest that ruminant genetics and physiology are correlated with microbiome structure and are potentially facilitated by specific heritable taxa that are phylogenetically related.