While high-temperature stress severely inhibits the growth, development, and tuberization of potatoes (Solanum tuberosum L.), moderate high temperatures can trigger thermomorphogenesis. However, the molecular mechanisms underlying thermomorphogenesis in potato remain largely elusive. In this study, we identified a heat-responsive, nucleus-plastid shuttling transcriptional activator, StHEMERA (StHMR), whose nuclear translocation was enhanced under high-temperature conditions. Transgenic analyses revealed that the high-temperature induced increase in plant height and cell elongation in potato depends on the function of StHMR. The StHMR-silenced lines displayed a phenotype insensitive to elevated temperatures. Biochemical evidence further revealed that StHMR forms a regulatory module with PHYTOCHROME INTERACTING FACTOR 4 (StPIF4), a potato homolog of the central Arabidopsis thermosensory. StPIF4 is indispensable for high-temperature-induced stem elongation and directly binds the promoters of the auxin biosynthesis gene YUCCA8 (StYUC8) and the cell-elongation gene α-EXPANSION A8 (StEXPA8). StPIF4 regulates cell elongation under high-temperature conditions by binding to E-box elements within the promoters of these genes. Notably, StHMR functions as a transcriptional co-activator that enhances the ability of StPIF4 to activate the transcription of StYUC8, especially under heat conditions. Collectively, this study characterizes the StHMR-StPIF4 module as a key molecular unit of potato thermomorphogenesis and highlights its potential relevance to tuber formation, providing promising molecular targets for breeding heat-tolerant potato varieties.