Many membranes must merge during cellular trafficking, but fusion and fission events initiating at exoplasmic (non-cytosolic) membrane surfaces are not well understood. Here we show that the C. elegans cell-cell fusogen anchor-cell fusion failure 1 (AFF-1) is required for membrane trafficking events during development of a seamless unicellular tube. EGF-Ras-ERK signaling upregulates AFF-1 expression in the excretory duct tube to promote tube auto-fusion and subsequent lumen elongation. AFF-1 is required for scission of basal endocytic compartments and for apically directed exocytosis to extend the apical membrane. Lumen elongation also requires the transcytosis factor Rab11, but occurs independently of dynamin and clathrin. These results support a transcytosis model of seamless tube lumen growth and show that cell-cell fusogens also can play roles in intracellular membrane trafficking events.