Plants adapt to warm environments through physiological and morphological changes termed thermomorphogenesis, which involve transcriptional reprogramming exerted mainly by PHYTOCHROME INTERACTING FACTOR 4 (PIF4). Fluctuating temperatures can also influence the patterns of cytosine DNA methylation, thereby influencing gene expression. However, whether these epigenetic changes provide an adaptative advantage remains unclear. Here, we provide evidence that DNA methylation is required to regulate thermomorphogenesis. Hypomethylated drm1 drm2 cmt3 mutants or seedlings treated with 5-azacytidine to block DNA methylation exhibit reduced hypocotyl growth at warm temperatures, primarily due to impaired cell elongation. Moreover, DNA hypomethylation compromises auxin biosynthesis and transport in response to warmth, partially by reducing PIF4 protein levels. Notably, the loss of DNA methylation leads to increased expression of SUPPRESSOR OF drm1 drm2 cmt3 (SDC), which in turn restricts hypocotyl elongation during thermomorphogenesis. Finally, we demonstrate that DNAme regulates the inhibition of SDC expression to promote gibberellin biosynthesis. Our findings underscore the critical role of DNA methylation in modulating gene expression in response to temperature fluctuations and provide new insights into the epigenetic regulation of thermomorphogenesis.