Herpesviruses are ubiquitous viral pathogens that infect all known vertebrates. It is estimated that over 90% of adults worldwide are infected with at least one of the nine human herpesviruses, which cause a wide range of morbidity and mortality. These viruses share a conserved assembly pathway, during which genome-containing capsids acquire a lipid envelope in a process called secondary envelopment. Herpes simplex virus (HSV)-1 proteins pUL7 and pUL51 form a complex that is involved in secondary envelopment, although their molecular function is not well understood. Neither pUL7 nor pUL51 share appreciable sequence-level homology with any protein of known function, which has frustrated attempts to infer their function by analogy. Since viral proteins can exhibit structural homology to other proteins in the absence of appreciable sequence conservation, the pUL7:pUL51 complex was characterised using small angle X-ray scattering and X-ray crystallography. pUL7:pUL51 forms a 1:2 heterotrimer in solution that dimerises at high concentrations. The crystal structure of the core pUL7:pUL51 heterodimer revealed that pUL7 has a novel fold. Immunoprecipitation experiments showed that the interaction between pUL7 and pUL51 homologues is conserved across multiple human herpesviruses, although the precise molecular details of the interface have diverged. Immunocytochemistry and fluorescence microscopy showed that localisation of pUL7 and pUL51 homologues to trans-Golgi network membranes is conserved, but only HSV-1 pUL7:pUL51 is recruited to focal adhesions. HSV-1 pUL51 structurally resembles endosomal sorting complex required for transport (ESCRT)-III components, a class of cellular proteins involved in membrane scission. HSV-1 pUL51 binds lipids when recombinantly expressed, and forms filamentous and ring-shaped polymers that resemble those formed by ESCRT-III superfamily proteins when purified. Sequence analysis of pUL71, the human cytomegalovirus pUL51 homologue, identified a C-terminal motif that resembles those involved in recruitment of the ATPase vacuolar protein sorting-associated protein 4 (VPS4) by ESCRT-III proteins. Prediction of the pUL71:VPS4 complex structure suggested that pUL71 binds to VPS4 via a short helix and a linear motif, in a similar manner to cellular interactors. The predicted structure was computationally validated using molecular dynamics simulations, which defined the contribution of key residues to the pUL71:VPS4 interaction. While other viruses are known to recruit ESCRT components to mediate membrane scission during virion assembly, this is the first example of structural mimicry of an ESCRT-III component and direct recruitment of VPS4 by a virus. These results provide a structural framework for understanding the role of the conserved pUL7:pUL51 complex in herpesvirus secondary envelopment.