Background <p>Improving feed efficiency in livestock is crucial for sustainable animal production. Residual feed intake (RFI) is a superior metric that accurately assesses feed efficiency. Animals with a low RFI (LRFI) usually consume less feed than animals with a high RFI (HRFI). Ruminal microbiota plays an important role in feed digestion in sheep. It is essential to elucidate the associations between rumen microbial composition, metabolic profiles, and growth performance of lambs with differing RFI by metagenomic sequencing and metabolomic profiling.</p> Results <p>Although no significant differences were observed in growth performance, LRFI lambs exhibited significantly lower dry matter intake (<i>P</i> &lt; 0.05) and improved feed efficiency. Integrative metagenomic and metabolomics analysis revealed that the LRFI group showed enrichment of bacteria (<i>Prevotella</i>, <i>Roseburia</i>, and <i>Pseudoscardovia</i>) (<i>P</i> &lt; 0.05) and metabolites (N-Acetylneuraminic acid 9-phosphate, N-Succinyl-L-glutamate, 5-hydroxyindolepyruvate, pelargonidin, sinapic acid, and spermidine) associated with efficient nitrogen metabolism, enhanced microbial protein synthesis, and antioxidant activity. By contrast, the HRFI group was characterized by increased abundance of microorganisms (<i>Methanobrevibacter</i>, <i>Ruminococcus</i>, <i>Butyrivibrio</i>, and <i>Sarcina</i>) (<i>P</i> &lt; 0.05), coupled with elevated levels of metabolites (histidinal, tetrahydrocorticosterone, and sakuranetin). Correlation networks identified positive correlations among <i>Prevotella</i>, unclassified <i>f_Prevotellaceae</i>, several amino acid intermediates and specific flavonoids, and the host traits of reduced DMI and RFI. Conversely, the genera <i>Methanobrevibacter</i>, <i>Ruminococcus</i>, <i>Butyrivibrio</i>, and <i>Sarcina</i> were positively correlated with the increased DMI and RFI.</p> Conclusions <p>Efficient (low-RFI) animals exhibited a <i>Prevotella</i>-driven microbiome and a distinct metabolome characterized by enrichment of several amino acid intermediates and specific flavonoids, while a more diverse but methanogen-related microbial community (such as <i>Methanobrevibacter</i>, <i>Ruminococcus</i>, <i>Butyrivibrio</i>, and <i>Sarcina</i>) is present in inefficient (HRFI) sheep. The identified microbial and metabolic profiles provide potential biomarkers for breeding feed-efficient animals and developing targeted nutritional interventions to improve ruminant production sustainability.</p>