Dynamic trimethylation of histone H3 at Lys27 (H3K27me3) affects gene expression and controls plant development and environmental responses. In Arabidopsis thaliana, RELATIVE OF EARLY FLOWERING 6/JUMONJI DOMAIN-CONTAINING PROTEIN 12 (REF6/JMJ12) demethylates H3K27me3 by recognizing a specific DNA motif; however, little is known about how REF6 activates target gene expression after recognition, especially in environmental responses. In response to warm ambient temperature, plants undergo thermomorphogenesis, which involves accelerated growth, early flowering, and changes in morphology. Here we show that REF6 regulates thermomorphogenesis and cooperates with the transcription factor PHYTOCHROMEINTERACTING FACTOR 4 (PIF4) to synergistically activate thermo-responsive genes under warm ambient temperature. The ref6 loss-of function mutants exhibited attenuated hypocotyl elongation at warm temperature, partially due to down-regulation of GIBBERELLIN 20-OXIDASE2 (GA20ox2) and BASIC HELIX-LOOP-HELIX 87 (bHLH87). REF6 enzymatic activity is necessary for warm ambient temperature responses. Together, our results provide direct evidence of an epigenetic modifier and a transcription factor working together to respond to the environment.