Fine tubes form inside cells as they reach their target tissues in epithelial ducts and in angiogenesis. Although a very suggestive model of cell hollowing proposes that intracellular lumen could arise by coalescence of intracellular vacuoles, how those tubes form in vivo remains an open question. We addressed this issue by examining intracellular lumen formation in the Drosophila trachea. The main branches of the Drosophila tracheal system have an extracellular lumen because their cells fold to form a tube. However, terminal cells, specialized cells in some of the main branches, form unicellular branches by the generation of an intracellular lumen. Conversely to the above-mentioned model, we find that the intracellular lumen arises by growth of an apical membrane inwards the cell. In support, we detect an appropriate subcellular compartmentalization of different components of the intracellular trafficking machinery. We show that both cellular elongation and lumen formation depend on a mechanism based on asymmetric actin accumulation and microtubule network organization. Given the similarities in the formation of fine respiratory tubes and capillaries, we propose that an inward membrane growth model could account for lumen formation in both processes.