Groundnut productivity and quality have been impeded by rising temperatures in semi-arid environments. Hence, understanding the effects and molecular mechanisms of heat stress tolerance will aid in tackling yield losses. In this context, a recombinant inbred line (RIL) population was developed and phenotyped for eight seasons at three locations for agronomic, phenological, and physiological traits under heat stress. A genetic map was constructed using genotyping-by-sequencing with 478 single-nucleotide polymorphism (SNP) loci spanning a map distance of 1,961.39 cM. Quantitative trait locus (QTL) analysis using phenotypic and genotypic data identified 45 major main-effect QTLs for 21 traits. Intriguingly, three QTL clusters (Cluster-1-Ah03, Cluster-2-Ah12, and Cluster-3-Ah20) harbor more than half of the major QTLs (30/45, 66.6%) for various heat tolerant traits, explaining 10.4%–38.6%, 10.6%–44.6%, and 10.1%–49.5% of phenotypic variance, respectively. Furthermore, important candidate genes encodingDHHC-type zinc finger family protein(arahy.J0Y6Y5),peptide transporter 1(arahy.8ZMT0C),pentatricopeptide repeat-containing protein(arahy.4A4JE9),Ulp1 protease family(arahy.X568GS),Kelch repeat F-box protein(arahy.I7X4PC),FRIGIDA-like protein(arahy.0C3V8Z), and post-illumination chlorophyll fluorescence increase(arahy.92ZGJC) were the underlying three QTL clusters. The putative functions of these genes suggested their involvement in seed development, regulating plant architecture, yield, genesis and growth of plants, flowering time regulation, and photosynthesis. Our results could provide a platform for further fine mapping, gene discovery, and developing markers for genomics-assisted breeding to develop heat-tolerant groundnut varieties.