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Heat stress compromises wheat (Triticum aestivium) resistance to Hessian fly (HF, Mayetiola destructor (Say)). This study aimed to investigate the impact of heat stress on transcript expression of wheat genes associated with resistance to HF infestation under normal and heat-stressed conditions. To this end, ‘Molly’, a wheat cultivar containing the resistance gene H13, was subjected to HF infestation, heat stress, and the combination of HF infestation and heat stress. Our RNA-Seq approach identified 21 wheat genes regulated by HF infestation under normal temperatures (18 °C) and 155 genes regulated by HF infestation when plants were exposed to 35 °C for 6 h. Three differentially expressed genes (DEGs) from the RNA-Seq analysis were selected to validate the gene function of these DEGs using the RT-qPCR approach, indicating that these DEGs may differentially contribute to the expression of wheat resistance during the early stage of wheat–HF interaction under various stresses. Moreover, the jasmonate ZIM domain (JAZ) gene was also significantly upregulated under these treatments. Our results suggest that the genes in heat-stressed wheat plants are more responsive to HF infestation than those in plants growing under normal temperature conditions, and these genes in HF-infested wheat plants are more responsive to heat stress than those in plants without infestation.