Golgi degradation by selective autophagy (Golgiphagy) requires receptors to direct Golgi fragments into phagophores for sequestration within autophagosomes, followed by lysosomal degradation. Here, we show that the Golgi transmembrane protein TM9SF3 is a receptor essential for Golgiphagy under nutrient stress and multiple Golgi stress conditions. TM9SF3 binds all six mammalian ATG8 proteins through its N-terminal LC3-interacting regions. TM9SF3 knockout blocks nutrient stress-induced Golgi fragmentation and reduces the targeting of Golgi fragments to autophagosomes, resulting in decreased Golgi protein degradation. Beyond nutrient stress, TM9SF3 is required for Golgiphagy induced by monensin and brefeldin A treatments, and disruptions in intra-Golgi protein glycosylation. Knockout of TM9SF3 and mutations in its LIRs both compromise protein glycosylation, whereas TM9SF3 overexpression promotes degradation of incompletely glycosylated proteins. Further, we show that TM9SF3 is required for breast cancer cell proliferation, and high TM9SF3 levels are associated with poor prognosis, implicating its function in breast cancer pathology.