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Wheat (Triticum aestivumL.) resistance to Hessian fly (HF,Mayetiola destructor) conferred by HF resistance (R) genes, is often vulnerable to heat stress. This study aims to investigate the molecular basis of heat-induced susceptibility in wheat to HF. We compared the resistant cultivar ‘Molly’, which carriesH13, with its susceptible near-isogenic line ‘Newton’ to determine how elevated temperature alters phenotypic and molecular responses to HF infestation. Our phenotyping results showed that a single 24 h heat treatment at 30 °C was sufficient to compromise Molly’s resistance, resulting in more than 70% of plants becoming susceptible. Transcriptomic profiling revealed that resistant Molly exhibited stronger and broader defenses than Newton under normal temperature, whereas heat-stressed Molly displayed extensive transcriptional reprogramming resembling the naturally susceptible Newton wheat. Comparative analysis of transcriptomic profiles identified 74 genes that are consistently regulated across all susceptible states at 24 h after initial HF infestation, including heat-stressed Molly and Newton under both high and normal temperatures, but not in the resistant Molly under normal temperature. Functional annotation of these susceptibility-related genes in combination with previous findings suggest that susceptibility is likely associated with increased auxin-related activity, reduced salicylic acid (SA) and OPDA-associated defense signaling, and altered coordination of defense pathways that favor feeding-site establishment and redirecting host resource to developing HF larvae. The identification of susceptibility-associated candidate genes provides molecular targets for breeding wheat cultivars with more durable resistance under rising temperatures.