Climate change poses a significant threat to global food security by adversely affecting chlorophyll content, photosystem II activity, grain yield, and reproductive development in finger millet, highlighting the need for functional genomics approaches in crop improvement. Despite extensive studies in major cereals, the molecular components and regulatory mechanisms underlying brassinosteroid (BR) biosynthesis and signalling remain unexplored in finger millet. This study aimed to determine how 24-epibrassinolide (EBR) enhances thermotolerance in finger millet seedlings by assessing its effects on physiological performance, antioxidant defence and by uncovering the underlying molecular mechanisms through transcriptomic reprogramming of stress-responsive genes. The findings revealed that elevated BR levels or signalling sustained survival, chlorophyll retention, and root development under heat stress by activating antioxidant defences and orchestrating transcriptomic reprogramming of stress-responsive pathways. Approximately 8 Gb of high-quality data were generated, assembling into 10,571 and 13,494 transcripts for heat-stressed control (HSControl) and heat-stressed EBR-treated (HSEBR), respectively. Functional annotation captured 75–88