Macroautophagic degradation is mediated by the sequestration of cellular material into double-membrane vesicles called autophagosomes, which subsequently fuse with the vacuole or lysosome to degrade the enclosed material. Autophagosomes are formed though the expansion of a membrane cisterna called the isolation membrane or phagophore. Although the mechanism underlying this membrane expansion has long remained unclear, recent studies have established that the lipid transfer protein complex Atg2-Atg18 tethers the isolation membrane to the endoplasmic reticulum (ER), and mediates lipid influx from the ER, thereby driving isolation membrane expansion. In Saccharomyces cerevisiae, the association of the Atg2-Atg18 complex with the isolation membrane has been reported to be mediated by Atg18 binding to phosphatidylinositol 3-phosphate and Atg2 binding to Atg9, both of which are present in the membrane. In addition, this complex has been suggested to associate with the ER via the N-terminal region of Atg2. However, how this complex, which otherwise disperses throughout the cytoplasm, associates with the ER upon autophagy induction remains unclear. Here, we identify an ER membrane protein that contributes to the association of Atg2 with the ER. This protein cooperates with the N-terminal region of Atg2 to mediate Atg2 targeting to the ER. The interaction between Atg2 and this protein is enhanced by phosphorylation of Atg2 by the Atg1 kinase, which is activated in response to autophagy induction at autophagosome formation sites, enabling the spatiotemporally regulated association of Atg2 with the ER.