ESCRT-III and IST1 proteins function in a variety of membrane fission reactions, including HIV budding, by cycling between two states: soluble monomers that can be recruited to different membranes, and higher-order assemblies that bind and remodel those membranes. In this paper, we show that the N-terminal core domains of IST1 and the ESCRT-III protein CHMP3 adopt the same structure, revealing that IST1 is a previously unrecognized member of the ESCRT-III family. In both cases, equivalent downstream helices fold back against the core, suggesting a mechanism for autoinhibition. Like the CHMP2A/CHMP3 pair, both IST1 and its binding partner, CHMP1B, can spontaneously assemble into helical tubes that may mimic ESCRT-III assemblies formed at membrane fission sites. Mutations that destabilize the core domain/autoinhibitory helix interaction activate these proteins for assembly in vitro and in vivo, revealing how ESCRT-III proteins switch between their soluble and assembled states.