Significance G-protein signaling contributes to nearly all aspects of cell physiology. In order for signaling to occur, the G-protein αβγ heterotrimer must be assembled from its individual subunits. The G-protein βγ subcomplex does not assemble spontaneously, but requires the protein-folding chaperone cytosolic chaperonin containing TCP-1 (CCT) and its cochaperone phosducin-like protein 1 (PhLP1). To understand the molecular mechanism underlying this process, we determined the structures of two key intermediates in Gβγ assembly, Gβ-CCT and PhLP1–Gβ-CCT, using cryo-electron microscopy and chemical cross-linking. These structures reveal the molecular basis for chaperone-mediated Gβγ assembly that can be exploited to design novel therapeutics to regulate G-protein signaling.