Phosducin-like protein (PhLP) has been shown to interact with the cytosolic chaperonin containing TCP-1 (CCT), and the βγ subunit dimer of heterotrimeric G proteins (Gβγ). Here we provide details obtained from cryo-electron microscopic and biochemical studies on the structure of the complex between the cytosolic chaperonin CCT and PhLP. Binding of PhLP to CCT occurs through only one of the two chaperonin rings, making multiple contacts with CCT through both its N- and C-terminal domains. In addition, we show that PhLP acts as a co-chaperonin along with CCT in mediating the assembly of the G protein βγ subunit and that assembly is dependant upon the phosphorylation of PhLP by the protein kinase CK2. Variants of PhLP lacking the CK2 phosphorylation sites, or variants with an inability to bind Gβγ block the assembly process and inhibit G protein signaling. PhLP forms a complex with CCT and nascent Gβ prior to the release of Gβγ from the ternary complex and subsequent association with the Gγ subunit to form the Gβγ dimer. In order to understand the mechanism of Gβγ dimer assembly and the role of PhLP phosphorylation in the assembly process, we provide here a method for the purification of the PhLP·CCT·Gβ ternary complex of sufficient purity for structural studies.