Plants are constantly challenged by a diversity of abiotic stressors, and growth arrest is a common plant response aimed at enhancing stress tolerance. Because of this growth/stress tolerance antagonism, plants must finely modulate their growth and responses to environmental stimuli. Here, we demonstrate that HSFB1, a heat shock transcription factor, plays a critical role in the coordination of plant growth and drought stress responses in Arabidopsis thaliana. First, we found that HSFB1 negatively regulates plant growth and development under normal conditions and that HSFB1 expression is enhanced under drought stress. Conversely, the loss-of-function mutant hsfb1 exhibited increased plant growth and reduced drought stress tolerance compared with the wild-type. Consistently, overexpression of HSFB1 suppressed plant growth and enhanced drought stress tolerance. Subsequently, via chromatin immunoprecipitation sequencing, RNA sequencing, and transient expression assays, we screened and identified the heat shock protein 101 (HSP101) gene as a direct transcriptional target of HSFB1. Genetic analysis suggested that HSP101 functions downstream of HSFB1 to positively regulate drought tolerance in plants. Furthermore, we found that HSFB1 physically interacts with the eukaryotic translation initiation factor eIF3G1, and this interaction appears to be further enhanced under drought stress. Notably, the mutation of eif3g1 increased the severity of drought-induced growth inhibition in the hsfb1 mutant, and eIF3G1 enhanced the transcriptional activation of HSFB1 on the HSP101 promoter under drought stress. Altogether, our findings highlight HSFB1 as a key regulator coordinating plant growth and drought stress responses in Arabidopsis.