Whereas recent studies in different species showed that the host genome shapes the microbial community profile, our new research strategy revealed substantial host genomic control of comprehensive functional microbial processes in the rumen of bovines by utilising microbial gene profiles from whole metagenomic sequencing. Of 1,107/225/1,141 rumen microbial genera/metagenome assembled uncultured genomes (RUGs)/genes identified, 203/16/352 were significantly (P<2.02 x10-5) heritable (0.13 to 0.61), revealing substantial variation in host genomic control. We found 29/22/115 microbial genera/RUGs/genes host-genomically correlated (-0.93 to 0.92) with emissions of the potent greenhouse gas methane (CH4), highlighting the strength of host genomic control of specific microbial processes impacting on CH4. Only one of these microbial genes was directly involved in methanogenesis (cofG), whereas others were involved in providing substrates for archaea (e.g. bcd and pccB), important microbial interspecies communication mechanisms (ABC.PE.P), host-microbiome interaction (TSTA3) and genetic information processes (RP-L35). In our population, selection based on abundances of the 30 most informative microbial genes provided a mitigation potential of 17% of mean CH4 emissions per generation, which is higher than for selection based on measured CH4 using respiration chambers (13%), indicating the high potential of microbiome-driven breeding to cumulatively reduce CH4 emissions and mitigate climate change.