Organelle fragmentation is crucial for the onset of autophagic programs that control lysosomal clearance of portions of organelles to be removed from cells. It is driven by membrane-bound organello-phagy receptors that display cytoplasmic intrinsically disordered modules (IDRs) containing short LC3-interacting regions (LIRs). Studies on ER-phagy receptors of the FAM134 family revealed the importance of transcriptional induction, and receptors phosphorylation, ubiquitylation and clustering for execution of the ER-phagy programs. In this model, ER fragmentation is promoted by the membrane-remodeling function of FAM134 reticulon homology domains (RHDs)18,19. However, RHDs are not conserved in ER-phagy receptors, nor in receptors for autophagy of other organelles that also require fragmentation such as the mitochondria. Thus, membrane remodeling by RHDs is unlikely to be a conserved mechanism to regulate organelle turnover. Here, we show that the membrane-tethering modules of ER-phagy receptors (RHDs for FAM134B, single/multi spanning transmembrane domains for TEX264 and SEC62) determine the sub-compartmental distribution of the receptors but are dispensable for ER fragmentation, regardless of their propensity to remodel the ER membrane. Our experiments reveal that the information encoding for ER fragmentation is contained in the cytoplasmic IDR modules of the ER-phagy receptors, which also control delivery of the ER fragments within degradative acidic compartments upon engagements of lipidated LC3/GABARAP proteins via their LIRs. Notably, the transplantation of ER-phagy receptors IDRs at the mitochondrial membrane induces DRP1-driven mitochondrial fragmentation and mitophagy, and the transplantation of mitophagy receptors IDRs at the ER membrane induces ER fragmentation and ER-phagy. Our work reveals the functional conservation of membrane-exposed IDRs in promoting organelle fragmentation and offers a method to control integrity and activity of intracellular organelles by surface activation of IDR modules with net negative charges.