Autophagy counterbalances endoplasmic reticulum (ER) expansion during the unfolded protein response (UPR). When the UPR is activated, yeast cells expand their ER volume by at least fivefold. This expansion is accompanied by the formation of autophagosome-like structures that selectively sequester and contain membrane stacks derived from the UPR-expanded ER. These structures, termed ER-containing autophagosomes (ERAs), are essential for cell survival under severe ER stress and do not require vacuolar proteases for their function. ER sequestration helps maintain a new steady-state level of ER abundance despite continuous accumulation of unfolded proteins. The UPR is a conserved ER-to-nucleus signaling pathway that adjusts ER abundance in response to unfolded proteins. It activates transcription factors that drive a comprehensive program to restore ER homeostasis. In yeast, the UPR is regulated by the Ire1 kinase, which activates the Hac1 transcription factor. The UPR also upregulates genes involved in protein folding, transport, and degradation. In metazoan cells, the UPR is regulated by multiple pathways, including Ire1, ATF6, and Perk. Autophagy is a process by which cells sequester and degrade cytoplasmic components, including organelles. It includes macroautophagy, which is non-selective, and selective forms such as pexophagy and mitophagy. ER-phagy, a selective form of autophagy, is activated during UPR-induced ER expansion. It involves the sequestration of ER membranes into autophagosome-like structures, which are then either sequestered or degraded. ER-phagy is essential for cell survival under severe ER stress and is not dependent on vacuolar proteases. The study shows that ER-phagy is activated by the UPR and is required for cell survival. It involves the sequestration of ER membranes into autophagosome-like structures, which are then either sequestered or degraded. ER-phagy is distinct from classical autophagy and is not dependent on vacuolar proteases. The study also shows that ER-phagy is not dependent on the Ire1 pathway and requires a second signal from the ER lumen. The findings suggest that ER-phagy is a physiologically important link between the UPR and autophagy. It helps maintain ER homeostasis by sequestering ER membranes and preventing the accumulation of unfolded proteins. The study also shows that ER-phagy is not dependent on the Ire1 pathway and requires a second signal from the ER lumen. The study provides new insights into the molecular mechanisms of ER-phagy and its role in maintaining ER homeostasis.Autophagy counterbalances endoplasmic reticulum (ER) expansion during the unfolded protein response (UPR). When the UPR is activated, yeast cells expand their ER volume by at least fivefold. This expansion is accompanied by the formation of autophagosome-like structures that selectively sequester and contain membrane stacks derived from the UPR-expanded ER. These structures, termed ER-containing autophagosomes (ERAs), are essential for cell survival under severe ER stress and do not require vacuolar proteases for their function. ER sequestration helps maintain a new steady-state level of ER abundance despite continuous accumulation of unfolded proteins. The UPR is a conserved ER-to-nucleus signaling pathway that adjusts ER abundance in response to unfolded proteins. It activates transcription factors that drive a comprehensive program to restore ER homeostasis. In yeast, the UPR is regulated by the Ire1 kinase, which activates the Hac1 transcription factor. The UPR also upregulates genes involved in protein folding, transport, and degradation. In metazoan cells, the UPR is regulated by multiple pathways, including Ire1, ATF6, and Perk. Autophagy is a process by which cells sequester and degrade cytoplasmic components, including organelles. It includes macroautophagy, which is non-selective, and selective forms such as pexophagy and mitophagy. ER-phagy, a selective form of autophagy, is activated during UPR-induced ER expansion. It involves the sequestration of ER membranes into autophagosome-like structures, which are then either sequestered or degraded. ER-phagy is essential for cell survival under severe ER stress and is not dependent on vacuolar proteases. The study shows that ER-phagy is activated by the UPR and is required for cell survival. It involves the sequestration of ER membranes into autophagosome-like structures, which are then either sequestered or degraded. ER-phagy is distinct from classical autophagy and is not dependent on vacuolar proteases. The study also shows that ER-phagy is not dependent on the Ire1 pathway and requires a second signal from the ER lumen. The findings suggest that ER-phagy is a physiologically important link between the UPR and autophagy. It helps maintain ER homeostasis by sequestering ER membranes and preventing the accumulation of unfolded proteins. The study also shows that ER-phagy is not dependent on the Ire1 pathway and requires a second signal from the ER lumen. The study provides new insights into the molecular mechanisms of ER-phagy and its role in maintaining ER homeostasis.