Significance Membrane asymmetry, curvature, and dynamics have major roles in cellular processes, including vesicle transport. The GTPase ADP ribosylation factor (Arf) and a lipid translocase (flippase) are critical for membrane reorganization during vesicle formation. Direct evidence that Arf and flippase work in concert on membrane transformation/architecture is, however, lacking. We demonstrate that activated Arf-like protein Arl1 interacts with the Arf-activating guanine nucleotide-exchange factor Gea2 and flippase Drs2, forming a ternary complex that is required for lipid asymmetry and Arl1 function at the Golgi. These findings represent a previously missing piece of the puzzle that is our understanding of Arf-mediated membrane remodeling.