Under long-term ecological stress, the Tarim wapiti (Cervus elaphus yarkandensis) has evolved unique adaptations in digestive physiology and energy metabolism. A multi-omics comparison of three Tarim wapiti and five Karakul sheep was used to examine the synergistic mechanism between rumen bacteria, short-chain fatty acids, and host epithelial regulation in order to clarify the mechanism of high roughage digestion efficiency in Tarim wapiti. Metagenomic sequencing (Illumina NovaSeq 6000) and gas chromatography revealed that Tarim wapiti exhibited significantly higher acetate and total VFA (TVFA) concentrations compared to Karakul sheep (p < 0.01), accompanied by lower ruminal pH and propionate levels. Core microbiota analysis identified Bacteroidetes (relative abundance: 52.3% vs. 48.1%), Prevotellaceae (22.7% vs. 19.4%), and Prevotella (18.9% vs. 15.6%) as dominant taxa in both species, with significant enrichment of Bacteroidetes in wapiti (p < 0.01). Functional annotation (PICRUSt2) demonstrated enhanced glycan biosynthesis (KEGG ko00511), DNA replication/repair (ko03430), and glycoside hydrolases (GH20, GH33, GH92, GH97) in wapiti (FDR < 0.05). Transcriptomic profiling (RNA-Seq) of rumen epithelium showed upregulated expression of SCFA transporters (PAT1: 2.1-fold, DRA: 1.8-fold, AE2: 2.3-fold; p < 0.01) and pH regulators (Na⁺/K⁺ ATPase: 1.7-fold; p < 0.05) in wapiti. Integrated analysis revealed coordinated microbial–host interactions through three key modules: (1) Bacteroidetes-driven polysaccharide degradation, (2) GHs-mediated fiber fermentation, and (3) epithelial transporters facilitating short-chain fatty acids absorption. These evolutionary adaptations, particularly the Bacteroidetes–short-chain fatty acids–transporter axis, likely underpin the wapiti’s superior roughage utilization efficiency, providing molecular insights for improving ruminant feeding strategies in an arid environment.