Selective autophagic clearance of mitochondria (mitophagy) is essential for development and cellular homeostasis. However, how phagophores acquire sufficient membrane to engulf large mitochondria remains poorly understood. Here, we studied the in situ architecture of forming mitophagosomes in developing Drosophila intestine using a combination of cryo-electron tomography (cryo-ET), cryo-focused ion beam (cryo-FIB) milling, serial lift-out and volume electron microscopy techniques. Our data reveal that the endoplasmic reticulum (ER) forms continuous membrane connections with the phagophore during mitophagosome formation. Additionally, ER-phagophore membrane continuities are increased and autophagosome membranes fail to close in Vps13D mutant enterocyte. Together, our findings support a model in which the ER directly fuses with the phagophore to facilitate rapid mitophagosome formation and reveal a novel function for Vps13D in mitophagosome membrane closure.