The endosomal sorting complex I required for transport (ESCRT‐I) is composed of the three subunits Vps23/Tsg101, Vps28 and Vps37. ESCRT‐I is recruited to cellular membranes during multivesicular endosome biogenesis and by enveloped viruses such as HIV‐1 to mediate budding from the cell. Here, we describe the crystal structure of a conserved C‐terminal domain from Sacharomyces cerevisiae Vps28 (Vps28‐CTD) at 3.05 Å resolution which folds independently into a four‐helical bundle structure. Co‐expression experiments of Vps28‐CTD, Vps23 and Vps37 suggest that Vps28‐CTD does not directly participate in ESCRT‐I assembly and may thus act as an adaptor module for downstream interaction partners. We show through mutagenesis studies that Vps28‐CTD employs its strictly conserved surface in the interaction with the ESCRT‐III factor Vps20. Furthermore, we present evidence that Vps28‐CTD is sufficient to rescue an equine infectious anaemia virus (EIAV) Gag late domain deletion. Vps28‐CTD mutations abolishing Vps20 interaction in vitro also prevent the rescue of the EIAV Gag late domain mutant consistent with a potential direct Vps28‐ESCRT‐III Vps20 recruitment. Therefore, the physiological relevant EIAV Gag–Alix interaction can be functionally replaced by a Gag‐Vps28‐CTD fusion. Because both Alix and Vps28‐CTD can directly recruit ESCRT‐III proteins, ESCRT‐III assembly coupled to Vps4 action may therefore constitute the minimal budding machinery for EIAV release.