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Lipoxygenase (LOX) is associated with responses to plant hormones, environmental stresses, and signaling substances. Methyl jasmonate (MeJA) treatment triggers the production of LOX, polyphenol oxidase, and protease inhibitors in various plants, producing resistance to herbivory. To examine the response of <i>MtLOX24</i> to MeJA, the phenotypic and physiological changes in <i>Medicago truncatula MtLOX24</i> overexpression and <i>lox</i> mutant plants were investigated. Additionally, wild-type R108, the <i>MtLOX24</i>-overexpressing line L4, and the mutant <i>lox-1</i> were utilized as experimental materials to characterize the differentially expressed genes (DEGs) and metabolic pathways in response to MeJA. The results indicate that after treatment with 200 µM of MeJA, the damage in the mutants <i>lox-1</i> and <i>lox-2</i> was more serious than in the overexpressing lines L4 and L6, with more significant leaf wilting, yellowing, and oxidative damage in <i>lox-1</i> and <i>lox-2</i>. Exogenous application of MeJA induced H₂O₂ production and POD activity but reduced CAT activity in the <i>lox</i> mutants. Transcriptome analysis revealed 10,238 DEGs in six libraries of normal-growing groups (cR108, cL4, and clox1) and MeJA-treated groups (R108, L4, and lox1). GO and KEGG functional enrichment analysis demonstrated that under normal growth conditions, the DEGs between the cL4 vs. cR108 and the clox-1 vs. cR108 groups were primarily enriched in signaling pathways such as plant–pathogen interactions, flavonoid biosynthesis, plant hormone signal transduction, the MAPK signaling pathway, and glutathione metabolism. The DEGs of the R108 vs. cR108 and L4 vs. cL4 groups after MeJA treatment were mainly enriched in glutathione metabolism, phenylpropanoid biosynthesis, the MAPK signaling pathway, circadian rhythm, and α-linolenic acid metabolism. Among them, under normal growth conditions, genes like PTI5, PR1, HSPs, PALs, CAD, CCoAOMT, and CYPs showed significant differences between L4 and the wild type, suggesting that the expression of these genes is impacted by <i>MtLOX24</i> overexpression. CDPKs, CaMCMLs, IFS, JAZ, and other genes were also significantly different between L4 and the wild type upon MeJA treatment, suggesting that they might be important genes involved in JA signaling. This study provides a reference for the study of the response mechanism of <i>MtLOX24</i> under MeJA signaling.