Heat stress poses a significant threat to global wheat (Triticum aestivum) production, causing substantial yield losses. Identifying heat tolerance genes and understanding their molecular mechanisms are crucial for improving wheat resilience. This study identifies a heat tolerance gene, TaSG-D1^286K, in Indian dwarf wheat (Triticum sphaerococcum), which encodes an STKc GSK3 kinase. The TaSG-D1^286K variant enhances heat tolerance by increasing the phosphorylation and stability of downstream target TaPIF4 under heat stress conditions. Evolutionary analysis reveals that TaPIF4 undergoes selective pressure during wheat breeding in China, with InDels predominantly occurring in the TaPIF4 promoter of modern Chinese cultivars, leading to decreased expression levels in response to heat stress. These findings provide insights into heat stress response mechanisms and suggest potential strategies to improve wheat heat tolerance.Heat stress poses a significant threat to global wheat (Triticum aestivum) production, causing substantial yield losses. Identifying heat tolerance genes and understanding their molecular mechanisms are crucial for improving wheat resilience. This study identifies a heat tolerance gene, TaSG-D1^286K, in Indian dwarf wheat (Triticum sphaerococcum), which encodes an STKc GSK3 kinase. The TaSG-D1^286K variant enhances heat tolerance by increasing the phosphorylation and stability of downstream target TaPIF4 under heat stress conditions. Evolutionary analysis reveals that TaPIF4 undergoes selective pressure during wheat breeding in China, with InDels predominantly occurring in the TaPIF4 promoter of modern Chinese cultivars, leading to decreased expression levels in response to heat stress. These findings provide insights into heat stress response mechanisms and suggest potential strategies to improve wheat heat tolerance.