Membrane trafficking is a highly coordinated process in eukaryotes essential for maintaining lipid homeostasis and sorting proteins to the proper location inside cells. The Golgi complex serves as the hub of this dynamic set of pathways where it directs cargo sorting through vesicle mediated transport. Vesicles of varying lipid composition loaded with different protein cargo are in constant flux through the Golgi and precise spatial and temporal regulation of these processes requires communication between compartments. Rab GTPases are small signaling proteins that act as molecular switches to regulate vesicular trafficking. Rab6 functions at the Golgi where it is important for endosome to Golgi retrograde transport in both yeast and metazoans and for anterograde exit from the TGN in metazoans. The Ric1-Rgp1 protein complex is a conserved guanine nucleotide exchange factor required for activation of Rab6. In mammalian cells Ric1-Rgp1 localization is thought to be regulated by the Rab33 GTPase, but it remains unresolved how Ric1-Rgp1 specifically recognizes Rab6 and the mechanism by which it catalyzes Rab6 nucleotide exchange. Furthermore, little is known about the structure and domain organization of Ric1-Rgp1. We have used cryo‐EM to determine the structure of the yeast Ric1-Rgp1‐Rab6 complex, representing the key intermediate of the nucleotide exchange reaction. This structure reveals the overall architecture of the complex and has enabled us to identify specific interactions that are critical for proper recognition and activation of Rab6 on the membrane surface. Our findings provide a detailed understanding of the molecular mechanisms underlying regulated Rab6 activation by the Ric1-Rgp1 complex and identify conserved structural elements in both proteins that are required for proper membrane association and function. Collectively, these results provide a structural basis for understanding how essential trafficking events in the secretory pathway are regulated at the molecular level.