Boron (B) toxicity is one of the major abiotic stresses limiting wheat productivity in arid and semi-arid regions of the world. Thus, it is important to understand the molecular basis of tolerance in boron-tolerant wheat genetic resources for effective breeding. Wild emmer wheat is a valuable genetic resource for tolerance to multiple abiotic stresses; however, the molecular mechanisms behind boron toxicity tolerance in this species has not been sufficiently characterized. Here, we present the first RNA sequencing-based transcriptomic analysis of B toxicity response in a boron-tolerant Triticum dicoccoides genotype, PI362036. Shoot tissues exposed to high boron (10 mM B) for 7 days showed extensive transcriptional reprogramming with 2783 differentially expressed genes. Functional enrichment analyses showed that B toxicity significantly altered the genes associated with biosynthesis of secondary metabolites, metabolic pathways, ribosomal activity, carbon metabolism, RNA transport, photosynthesis-antenna proteins, and citrate cycle pathway. Several transcription factor families, including TIG, MYB, MYB-related families, NAC, C2H2-GATA, ARF, and AP2-EREBP families, showed significant differential regulation, emphasizing their regulatory roles in B stress adaptation. Collectively, this study provides the first comprehensive transcriptomic framework of boron toxicity tolerance in T. dicoccoides under short-term high boron exposure, identifying candidate genes and pathways that may be exploited for improving boron tolerance in cultivated wheat through targeted breeding strategies. Given that boron toxicity in agricultural systems primarily arises from excessive boron accumulation in soils and irrigation water, the identified pathways offer insight into early adaptive responses of shoot tissues to elevated boron availability.