Timely growth cessation before winter is crucial for the survival of perennial plants in temperate and boreal regions. Short photoperiod (SP) and low temperature (LT) are major seasonal cues regulating growth cessation. SP, sensed in the leaves, initiates growth cessation by downregulating FLOWERING LOCUS T 2(FT2) expression, but how LT regulates seasonal growth is unclear. Genetic and cell biological approaches identified a hybrid aspen EARLY FLOWERING 3(ELF3) ortholog with a prion-like domain (PrLD) that undergoes LT-responsive phase separation as a key mediator of LT-induced growth cessation. In contrast with SP, LT acts independently of FT2 downregulation and targets the AIL1-BRC1 transcription factor network and hormonal pathways via ELF3 to induce growth cessation. Intriguingly, ELF3 also functions in SP-mediated growth cessation by downregulating FT2 in leaves. Our work thus reveals a previously unrecognized role of ELF3 in growth cessation and in coordinating temperature and photoperiodic pathways to enable robust adaptation to seasonal change.