Iron (Fe) deficiency limits legume productivity, yet the role of microbiome in overcoming this is understudied. In this study, the colonization ofTrichoderma afroharzianumT22 in roots of Fe-deficient pea cultivars varied. In Sugar Snap,T22enhanced growth parameters consistent with increased tissue Fe and rhizosphere siderophore under Fe deficiency. Interestingly, T22 showed an increased abundance of 16S bacterial community, particularlyRhizobium leguminosarumandRhizobium indicumalong with upregulation ofNifA,NifD,andNifHin nodules, suggesting a connection between T22 and rhizobia in Fe-starved pea. The split-root assay demonstrated systemic signaling between T22 and the host, promoting Fe deficiency tolerance. RNA-seq analysis showed 575 and 818 differentially expressed genes upregulated and downregulated in roots of Fe-deficient pea inoculated with T22. The upregulated genes (monooxygenase activity, ammonia-lyase activity, 4-coumarate-CoA ligase) are involved in flavonoid biosynthesis, along with genes related to mineral transport and redox homeostasis. A flavonoid precursor restored plant health even in the absence of T22, thereby promoting microbial symbiosis in mitigating Fe deficiency. Further, the elevation of siderophores and root flavonoids diminished when T22 was substituted with Fe, eliminating the need for microbiome-driven Fe enhancement which was supported by the higher growth ofR. leguminosarumco-cultured with T22 in Fe-deficient media. Hence, the beneficial effect of T22 on rhizobia likely results from their interactions, rather than from improved Fe status of plants. This study provides the first mechanistic insights into T22 interactions with hosts and rhizobia, proposing microbiome strategies to alleviate Fe deficiency in peas and other legumes.