The endoplasmic reticulum (ER) is a cellular organelle responsible for protein synthesis and folding. When the protein folding capacity is exceeded, unfolded or misfolded proteins accumulate, causing ER stress and triggering the unfolded protein response (UPR) to restore ER proteostasis. Although UPR genes in plants are expressed in a diel cycle, the mechanisms by which the circadian clock regulates these genes are not well understood. Here, we demonstrate that ER stress sensitivity in root growth exhibits time-of-day phases and that the circadian clock regulates the expression of UPR target genes during ER stress. Notably, mutations in the core morning clock component CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) impair ER stress recovery. CCA1 forms a complex with the UPR modulator bZIP28 and acts as upstream regulator in ER stress recovery. Upon ER stress, CCA1 is stabilized and associates with bZIP28 at the ER stress response element of the BiP3 promoter, enhancing the ER stress response. Thus, CCA1 coordinates a time-dependent adaptive response to ER stress with bZIP28 to maintain ER proteostasis. Our results suggest that the circadian clock primes the timing and levels of ER chaperone expression to enhance ER stress tolerance.