ABSTRACT Ruminant livestock farming is vital for food security, although being a major source of methane, a key greenhouse gas. The ruminant microbiome is pivotal for nutrient digestion, animal health, and enteric methane mitigation. Genome‐resolved metagenomics is an effective approach for exploring microbial communities and functions, yet existing global catalogs of ruminant microbial genomes remain notably incomplete. To address this gap, we collected a compilation of 3567 metagenomic samples from 18 ruminant species across 27 countries to construct the ruminant gastrointestinal metagenome‐assembled genomes (MAG) catalog (RGMC). We obtained a total of 40,812 non‐redundant MAGs at the strain level, spanning 53 bacterial classes and 4 archaeal classes, which represents the most comprehensive database of its kind to date, greatly exceeding the Bovine Gastro Microbial Genome Map (BGMGM). Importantly, we systematically resolved the metabolic potential of prokaryotic MAGs, with detailed profiling of pathways such as carbohydrate utilization and hydrogen metabolism. In direct response to the challenge of enteric methane emissions, we identified and annotated 1082 hydrogenotrophic bacteria and 697 methanogenic archaea, key microbial groups governing hydrogen flux and methanogenesis. By providing this functionally characterized, strain‐resolved resource, the RGMC advances our capacity to investigate and ultimately modulate the ruminant gastrointestinal microbiome for enhanced sustainability.