Climate warming poses increasing thermal challenges to plants, yet how plasma membrane biophysics contributes to heat adaptation remains poorly understood. In this work, we showed that the malectin-like receptor kinase FERONIA (FER) acts as a membrane-anchored thermal switch in Arabidopsis. FER organizes sterol-dependent nanoclusters that control heat acclimation. Moderate heat activated FER through the RAPID ALKALINIZATION FACTOR 34 (RALF34) peptide and promoted its recruitment to sterol-rich nanodomains. There, FER nucleated dynamic nanoclusters enriched in stress-signaling components. These nanoclusters stabilized liquid-ordered membrane phases and activated heat shock transcription factor-heat shock protein signaling, enhancing thermotolerance. However, under extreme heat the nanoclusters rapidly disassembled, preventing maladaptive responses. Our findings thus establish nanoscale membrane compartmentalization as a key mechanism linking lipid dynamics to plant thermal resilience.