Biosynthetic traffic drives plasma membrane growth. For early cleavage of the Drosophila embryo, this growth is rapid, but regulated, for repeated cycles of furrow ingression and regression. We report that furrow ingression requires Asap, a conserved Arf GTPase activating protein (GAP). Although Asap has several known effects, our genetic analyses argued that furrow loss with asap RNAi was linked predominantly to reduced Arf1 function at the Golgi. Moreover, Arf1 levels at the Golgi displayed a direct relationship with total cellular levels of Asap. Although Asap lacks Golgi enrichment, a conserved residue for Arf1 regulation by Asap was required for Golgi organization and output. We propose that Asap maintains Arf1 activity at the Golgi by recycling Arf1 from post-Golgi compartments. This role appears essential for cell division, and is thus unlike the roles of characterized Golgi Arf GAPs which act redundantly for cell viability. Strikingly, Asap re-localized to the nuclear region at metaphase, a shift that coincided with transient Golgi re-organization preceding cleavage furrow regression. Thus, we further propose that Asap sequestration underlies periods of Golgi attenuation and furrow regression during the cell cycle.