Autophagy eliminates cytoplasmic material by engulfment in membranous vesicles targeted for lysosome degradation. Nonselective autophagy coordinates sequestration of bulk cargo with the growth of the isolation membrane (IM) in a yet-unknown manner. Here, we show that in the budding yeast Saccharomyces cerevisiae, IMs expand while maintaining a rim sufficiently wide for sequestration of large cargo but tight enough to mature in due time. An obligate complex of Atg24/Snx4 with Atg20 or Snx41 assembles locally at the rim in a spatially extended manner that specifically depends on autophagic PI(3)P. This assembly stabilizes the open rim to promote autophagic sequestration of large cargo in correlation with vesicle expansion. Moreover, constriction of the rim by the PI(3)P-dependent Atg2-Atg18 complex and clearance of PI(3)P by Ymr1 antagonize rim opening to promote autophagic maturation and consumption of small cargo. Tight regulation of membrane rim aperture by PI(3)P thus couples the mechanism and physiology of nonselective autophagy. Display omitted •The nonselective yeast phagophore expands spherically while maintaining a narrow rim•The Atg2-Atg18 complex maintains rim constriction during membrane expansion•Local assembly of an autophagy-specific Atg20-Atg24 stabilizes a widely open rim•Rim stabilization is essential for autophagic sequestration of large cytoplasmic cargo Autophagosome biogenesis couples sequestration of cargo to expansion of the autophagic membrane in an elusive manner. Shatz et al. show that the rim of the nonselective yeast phagophore is tightly regulated to balance the inclusion of large cytoplasmic cargo with productive maturation in due time.