<jats:title>SUMMARY</jats:title><jats:p>Proteostasis of the endoplasmic reticulum (ER) is controlled by sophisticated signaling pathways that are collectively called the unfolded protein response (UPR) and are initiated by specialized ER membrane‐associated sensors. The evidence that complete loss‐of‐function mutations of the most conserved of the UPR sensors, inositol‐requiring enzyme 1 (IRE1), dysregulates tissue growth and development in metazoans and plants raises the fundamental question as to how IRE1 is connected to organismal growth. To address this question, we interrogated the Arabidopsis primary root, an established model for organ development, using the tractable Arabidopsis IRE1 mutant <jats:italic>ire1a ire1b</jats:italic>, which has marked root development defects in the absence of exogenous stress. We demonstrate that IRE1 is required to reach maximum rates of cell elongation and root growth. We also established that in the actively growing <jats:italic>ire1a ire1b</jats:italic> mutant root tips the Target of Rapamycin (TOR) kinase, a widely conserved pro‐growth regulator, is hyperactive, and that, unlike cell proliferation, the rate of cell differentiation is enhanced in <jats:italic>ire1a ire1b</jats:italic> in a TOR‐dependent manner. By functionally connecting two essential growth regulators, these results underpin a novel and critical role of IRE1 in organ development and indicate that, as cells exit an undifferentiated state, IRE1 is required to monitor TOR activity to balance cell expansion and maturation during organ biogenesis.</jats:p>