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Global warming-associated increases in temperature, particularly at nighttime, are detrimental to rice grain filling, ultimately leading to losses in grain weight. However, the molecular mechanisms associated with grain weight loss in rice exposed to high nighttime temperature stress are poorly understood. To screen the genes and single nucleotide polymorphisms (SNPs) associated with high nighttime temperature stress in rice, a hybrid sequencing strategy was used to analyze the differentially expressed genes and SNPs between two rice coisogenic strains, a heat-tolerant strain (HTS) and heat-sensitive strain (HSS), following short-term extreme high nighttime temperature stress at the first stage of seed ripening. Ultimately, 56 genes were differentially expressed between HTS and HSS. After short-term extreme high nighttime temperature stress, genes involved in photosynthesis, oxidation, and detoxication by glutathione were upregulated in HSS in comparison to HTS, while that of the heat response-related transcription factor genes were significantly upregulated in HTS in comparison to HSS. Unique SNPs located on the genes peroxidase precursor, glutathione S-transferase GSTU6, glycosyl hydrolases, carboxyvinylcarboxyphosphonate phosphorylmutase, and prolamin precursor PROLM3 were present in HTS but absent from HSS and showed slight alterations in gene expression between HTS and HSS. The proposed model indicated that high nighttime temperature enhanced cellular respiration, disturbed the oxidant-antioxidant balance, and consumed energy-rich substances, ultimately leading to reduced grain yield in HSS in contrast to HTS. These genes and unique SNPs provide genetic resources for the breeding of heat-tolerant rice varieties, and the model provides insights into the molecular basis of the response of rice to high nighttime temperature stress.