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Meat and milk from ruminants provide an important source of protein and other nutrients for human consumption. Although ruminants have a unique advantage of being able to consume forages and graze lands not suitable for arable cropping, 2% to 12% of the gross energy consumed is converted to enteric CH4 during ruminal digestion, which contributes approximately 6% of global anthropogenic greenhouse gas emissions. Thus, ruminant producers need to find cost-effective ways to reduce emissions while meeting consumer demand for food. This paper provides a critical review of the substantial amount of ruminant CH4-related research published in past decades, highlighting hydrogen flow in the rumen, the microbiome associated with methanogenesis, current and future prospects for CH4 mitigation and insights into future challenges for science, governments, farmers and associated industries. Methane emission intensity, measured as emissions per unit of meat and milk, has continuously declined over the past decades due to improvements in production efficiency and animal performance, and this trend is expected to continue. However, continued decline in emission intensity will likely be insufficient to offset the rising emissions from increasing demand for animal protein. Thus, decreases in both emission intensity (g CH4/animal product) and absolute emissions (g CH4/day) are needed if the ruminant industries continue to grow. Providing producers with cost-effective options for decreasing CH4 emissions is therefore imperative, yet few cost-effective approaches are currently available. Future abatement may be achieved through animal genetics, vaccine development, early life programming, diet formulation, use of alternative hydrogen sinks, chemical inhibitors and fermentation modifiers. Individually, these strategies are expected to have moderate effects (<20% decrease), with the exception of the experimental inhibitor 3-nitrooxypropanol for which decreases in CH4 have consistently been greater (20% to 40% decrease). Therefore, it will be necessary to combine strategies to attain the sizable reduction in CH4 needed, but further research is required to determine whether combining anti-methanogenic strategies will have consistent additive effects. It is also not clear whether a decrease in CH4 production leads to consistent improved animal performance, information that will be necessary for adoption by producers. Major constraints for decreasing global enteric CH4 emissions from ruminants are continued expansion of the industry, the cost of mitigation, the difficulty of applying mitigation strategies to grazing ruminants, the inconsistent effects on animal performance and the paucity of information on animal health, reproduction, product quality, cost-benefit, safety and consumer acceptance.