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SUMMARY: Wheat growth process has been experiencing severe challenges arising from the adverse environment. Notably, the incidence of Fusarium crown rot (FCR), a severe soil‐borne disease caused by Fusarium pseudograminearum (Fp), has significantly intensified in various wheat‐growing regions, resulting in a decline in grain yield. However, the identification of wheat varieties and the exploration of effective gene resources resistant to FCR have not yet been accomplished. Here, we screened and identified the tryptophan metabolism pathway to participate in wheat resistance to FCR by correlation analysis between transcriptome and metabolome, and found that indole‐3‐acetaldehyde (IAAld) and melatonin, two key metabolites in the tryptophan metabolic pathway, were significantly accumulated in Fp‐induced wheat stem bases. Interestingly, exogenous application of these two metabolites could significantly enhance wheat resistance against Fp. Additionally, we observed that the activity of TaALDHase, a crucial enzyme responsible for catalyzing IAAld to produce indole‐3‐acetic acid (IAA), was inhibited. Conversely, the activity of TaMTase, a rate‐limiting involved in melatonin biosynthesis, was enhanced in the Fp‐induced wheat transcriptome. Further analysis showed that TaWRKY24 could regulate IAA and melatonin biosynthesis by inhibiting the expression of TaALDHase and enhancing the transcription of TaMTase, respectively. Silencing of TaALDHase could significantly increase wheat resistance to FCR. However, interference with TaWRKY24 or TaMTase could decrease wheat resistance to FCR. Collectively, our findings demonstrate the crucial role of the tryptophan metabolism pathway in conferring resistance against FCR in wheat, thereby expanding its repertoire of biological functions within the plant system. Significance Statement: We utilized an integrated multi‐omics analysis to elucidate the regulatory role of a crucial metabolic pathway in conferring resistance against Fusarium crown rot in wheat. Our study demonstrates that the TaWRKY24 gene in wheat acts as a central hub, orchestrating key genes involved in the tryptophan metabolic pathway and actively participating in defense mechanisms against Fusarium crown rot. By downregulating these genes and modulating metabolites regulated by them, we enhance the disease resistance of wheat. [ABSTRACT FROM AUTHOR]