Soil-borne Fusarium wilt imposes substantial economic losses on agriculture, with Vicia faba exhibiting pronounced susceptibility to Fusarium disease. However, the mechanisms underlying V. faba's resistance to Fusarium and the intricate interplay between crucial rhizosphere microbes and root exudates during pathogen attack remain inadequately understood. This study investigates the interaction between faba bean plants and the soil microbiome to elucidate the mechanisms underlying plant Fusarium wilt. Through comprehensive analysis of 16S ribosomal RNA gene and internal transcribed spacer (ITS) sequencing data obtained from the faba bean rhizosphere soil, this research successfully identified key microbial groups that are enriched in the disease-suppressing rhizosphere, namely Bacillus, Pseudomonas, and Trichoderma. The strains displayed significant inhibitory effects on Fusarium oxysporum, notably. A synthetic community was constructed using these strains, which exhibited a remarkable capacity to suppress Fusarium wilt in faba bean seedlings, achieving an impressive inhibition rate of up to 71.76%. Non-targeted metabolomics analysis was employed to uncover the metabolic pathways through which this Synthetic community aids plants in resisting pathogens. Additionally, metagenomic analysis revealed an increased abundance of Antibiotic Resistance Genes (ARGs) in the rhizosphere soil of diseased plants, while the soil associated with healthy plants exhibited enhanced activity in nitrogen fixation, nucleotide metabolism, and carbohydrate metabolism pathways. Soil metabolites and root exudates were analyzed, and a Random Forest model was employed to investigate the impact of exogenous metabolites on Fusarium wilt occurrence. Significantly, compounds such as 10 µM Betaine, Proline, and Racemosin demonstrated remarkable efficacy in reducing the incidence of Fusarium wilt. Furthermore, transcriptomic and non-targeted metabolomics analyses were conducted in this study, revealing substantial enrichment in pathways including jasmonic acid metabolism, alanine metabolism, aspartate metabolism, glutamate metabolism, and unsaturated fatty acid biosynthesis in diseased V. faba. This study not only advances our understanding of plant Fusarium wilt and their impact mechanisms but also provides valuable insights for enhancing soil health and crop disease resistance.