One of the primary events that must occur repeatedly throughout a complex animal’s lifetime is the ingression of a plasma membrane furrow. Furrow formation and ingression are obligate parts of cell division, and drive the physical separation of one cell into two cells. Furrow formation in early syncytial Drosophila embryos is exceptionally rapid, with hundreds of furrows forming synchronously in as little as 4 minutes. Here, we use 4D imaging to identify furrow formation, stabilization, and regression periods, and identify a rapid, membrane-dependent pathway that is essential for plasma membrane furrow formation in vivo. While Myosin II function is thought to provide the ingression force for cytokinetic furrows, the role of membrane trafficking pathways in guiding furrow formation is less clear. We demonstrate that a membrane trafficking pathway centered on RalA, Rab8, Rab11, and the exocyst complex is required for fast furrow ingression in the early fly embryo. This trafficking pathway is absolutely required for furrow formation and initiation, and genomic instability occurs when its function is disrupted. We show that Rab8 vesicular intermediates direct the delivery of internal cytoplasmic Rab11 membrane pools to the cell surface through a RalA/exocyst targeting function. In contrast, Myosin II activity is not required for furrow ingression, but is needed to enforce furrow uniformity. These studies identify a pathway, which stretches from Rab11 to Rab8 to RalA and the exocyst complex that mediates rapid furrow formation in early Drosophila embryos.