Ruminants are important for global food security but are major sources of the greenhouse gas methane. Methane yield is controlled by the cycling of molecular hydrogen (H2), which is produced during carbohydrate fermentation and consumed by methanogenic, acetogenic, and respiratory microorganisms. However, we lack a holistic understanding of the mediators and pathways of H2 metabolism, and how this varies between ruminants with different methane-emitting phenotypes. Here we used metagenomic, metatranscriptomic, metabolomics, and biochemical approaches to compare H2 cycling and reductant disposal pathways between low-methane-yield Holstein and high-methane-yield Jersey dairy cattle. The microbiota of Holstein cattle disposed of reductant via propionate and amino acid production and expressed uptake [NiFe]-hydrogenases to use H2 to support sulfate and nitrate respiration. In contrast, Jersey microbiota primarily disposed of H2 through methanogenesis via methanogenic [NiFe]-hydrogenases and acetogenesis via [FeFe]-hydrogenases, resulting in enhanced methane and acetate production. These findings were supported by two in vitro measurements of microbiota activities and metabolites, as well as public global rumen microbiome data from sheep and beef cattle. Overall, this study highlights the importance of promoting alternative H2 consumption and reductant disposal pathways for the synthesis of host-beneficial metabolites and the reduction of methane production in ruminants.