Acanthamoeba-infecting Mimiviridae belong to three clades: Mimiviruses (A), Moumouviruses (B) and Megaviruses (C). The uniquely complex mobilome of these giant viruses includes virophages and linear 7 kb-DNA molecules called “transpovirons”. We recently isolated a new virophage (Zamilon vitis) and two new transpovirons (maBtv and mvCtv) respectively associated to B-clade and C-clade Mimiviridae. We used the capacity of the Zamilon virophage to replicate both on B-clade and C-clade host viruses to investigate the three partite interaction network governing the propagation of transpovirons. We notably performed proteomic comparisons of host viruses and virophage particles carrying or cleared of transpovirons in search of proteins involved in this adaptation process. These experiments revealed that transpoviron-encoded proteins are synthetized during the combined Mimiviridae/virophage/transpoviron replication process and are specifically incorporated into the virophage and Mimiviridae virions together with the cognate transpoviron DNA. This is a unique example of intricate commensalism in the viral world, where the Zamilon virophage and the transpoviron depend on their host giant virus to replicate, and the transpoviron depends on the virophage to propagate from one host virus to another.