Endoplasmic reticulum (ER) membrane contact sites (MCSs) mark positions where endosomes undergo fission for cargo sorting. To define the role of ER at this unique MCS, we targeted a promiscuous biotin ligase to cargo-sorting domains on endosome buds. This strategy identified the ER membrane protein TMCC1, a member of a conserved protein family. TMCC1 concentrates at the ER-endosome MCSs that are spatially and temporally linked to endosome fission. When TMCC1 is depleted, endosome morphology is normal, buds still form, but ER-associated bud fission and subsequent cargo sorting to the Golgi are impaired. We find that the endosome-localized actin regulator Coronin 1C is required for ER-associated fission of actin-dependent cargo-sorting domains. Coronin 1C is recruited to endosome buds independently of TMCC1, while TMCC1/ER recruitment requires Coronin 1C. This link between TMCC1 and Coronin 1C suggests that the timing of TMCC1-dependent ER recruitment is tightly regulated to occur after cargo has been properly sequestered into the bud. Display omitted •Targeted BioID identifies new family of ER-endosome MCS proteins termed TMCC•TMCC1 localizes to dynamic ER domains that define the position of endosome fission•TMCC1 regulates ER recruitment to endosome sorting domains for bud fission•Coronin1C at buds is a receptor for TMCC1-dependent ER recruitment to endosomes The timing and location of endosome fission is tightly regulated by TMCC1-mediated ER recruitment to ER-membrane contact to ensure that budding happens only after cargo has been properly sequestered.