Conserved by all domains of life, the endosomal sorting complex required for transport (ESCRT) machinery mediate membrane remodeling in numerous processes in cells including plasma membrane separation during cell division and reformation the nuclear membrane in post mitotic cells. The recent identification of ESCRT homologs in the Asgard archaeal superphyla, which is currently considered as the closest ancestor of eukaryotes, suggest a role for ESCRTs in the membrane remodeling processes that occurred during eukaryogenesis. Yet, the function of these distant ESCRT homologs is mostly unresolved. Here we show that Asgard ESCRT-III proteins, encoded by the Loki archaea, self-assemble into homo- and hetero- helical tubes, a hallmark of the eukaryotic ESCRT system. Asgard ESCRT-III tube assembly was enhanced in the presence of oligonucleotides and inhibited upon DNAase treatment. Notably, Loki-ESCRT-III helical tubes deformed and remodeled eukaryotic-like membrane vesicles, also in the presence of oligonucleotides. Collectively, our data indicate an ancient role for the ESCRT complex in membrane remodeling that may involve DNA binding and highlight core features of the ESCRT system that are conserved in both archaea and eukaryotes. The ability of Asgard archaeal ESCRTs to remodel eukaryotic-like membranes, place them at the junction between prokaryotes and eukaryotes, substantiating a role for the ESCRT system in eukaryogenesis.