The yeast SNX4 family of sorting nexins containing a BAR domain (SNX-BARs), Snx4/Atg24, Snx41, and Snx42/Atg20, are components of endocytic recycling and autophagy trafficking pathways. We show that these proteins possess membrane remodeling activity in vitro and coat endosome-derived transport carriers in vivo. Endosomes decorated by Snx4 proteins are also decorated with retromer SNX-BARs, but each SNX-BAR coats a distinct carrier that buds from the endosome, indicating that, in contrast to current models, the SNX4 and retromer pathways originate from a common endosome. Cells lacking Snx4 family proteins display a modest deficiency in autophagy that is severely exacerbated when mitochondrial phosphatidylethanolamine synthesis is ablated. Under these conditions, the lipid content of endosome-related organelles is perturbed and autophagosomes accumulate within the cytoplasm as a result of deficient fusion with the lysosome-like vacuole. SNARE-mediated autophagosome-vacuole fusion is restored by increasing phosphatidylethanolamine biosynthesis via alternative pathways, revealing a role for sorting nexins in controlling local pools of glycerophospholipids.