Balancing growth and stress resilience remains a central challenge in breeding stress-resistant crops. Here, we identify TOGR3 (THERMOTOLERANT GROWTH REQUIRED 3), which encodes the rice 26S proteasome β4 subunit, as a key regulator coordinating these two processes. Ubiquitylome profiling reveals that the TOGR3-dependent ubiquitin-proteasome system (UPS) maintains sugar homeostasis by selectively controlling the turnover of sugar-metabolizing enzymes. This regulation promotes leaf sugar accumulation, which serves dual roles by supplying carbon to sustain growth and by optimizing stomatal development and aperture dynamics to enhance leaf cooling capacity. Together, these mechanisms synergistically promote thermal-adaptive growth and thermotolerance in rice. Notably, combined overexpression of TOGR3 with the α2 subunit gene TT1 further enhances heat resistance, underscoring the potential of coordinated proteasome subunit engineering for crop improvement. Our findings uncover a regulatory module that fine-tunes the trade-off between plant growth and abiotic stress resilience, providing promising molecular targets for breeding climate-resilient crops.