Autophagic degradation of the endoplasmic reticulum (ER-phagy) is triggered by ER stress in diverse organisms. However, molecular mechanisms governing ER stress-induced ER-phagy remain insufficiently understood. Here we report that ER stress-induced ER-phagy in the fission yeast Schizosaccharomyces pombe requires Epr1, a soluble Atg8-interacting ER-phagy receptor. Epr1 localizes to the ER through interacting with integral ER membrane proteins VAPs. Bridging an Atg8-VAP association is the main ER-phagy role of Epr1, as it can be bypassed by an artificial Atg8-VAP tether. VAPs contribute to ER-phagy not only by tethering Atg8 to the ER membrane, but also by maintaining the ER-plasma membrane contact. Epr1 is upregulated during ER stress by the unfolded protein response (UPR) regulator Ire1. Loss of Epr1 reduces survival against ER stress. Conversely, increasing Epr1 expression suppresses the ER-phagy defect and ER stress sensitivity of cells lacking Ire1. Our findings expand and deepen the molecular understanding of ER-phagy. Display omitted •Epr1 is a soluble ER-phagy receptor critical for ER stress-induced ER-phagy•The main role of Epr1 is to bridge the association between Atg8 and VAPs•VAP-mediated ER-plasma membrane contact is important for ER stress-induced ER-phagy•UPR regulator Ire1 contributes to ER stress-induced ER-phagy by upregulating Epr1 Zhao et al. show that the fission yeast protein Epr1 confers resistance to ER stress by promoting the autophagic degradation of the ER (ER-phagy). Epr1 acts as a bridging molecule to mediate the association between Atg8 on the autophagic membrane and the integral membrane proteins VAPs on the ER.