Epithelial tubes in developing organs, such as mammalian lungs and insect tracheae, need to expand their initially narrow lumina to attain their final, functional dimensions. Despite its critical role for organ function, the cellular mechanism of tube expansion remains unclear. Tracheal tube expansion in Drosophila involves apical secretion and deposition of a luminal matrix, but the mechanistic role of secretion and the nature of forces involved in the process were not previously clear. Here we address the roles of cell-intrinsic and extrinsic processes in tracheal tube expansion. We identify mutations in the sec24 gene stenosis, encoding a cargo-binding subunit of the COPII complex. Via genetic-mosaic analyses, we show that stenosis-dependent secretion drives tube expansion in a cell-autonomous fashion. Strikingly, single cells autonomously adjust both tube diameter and length by implementing a sequence of events including apical membrane growth, cell flattening, and taenidial cuticle formation. Known luminal components are not required for this process. Thus, a cell-intrinsic program, rather than nonautonomous extrinsic cues, controls the dimensions of tracheal tubes. These results indicate a critical role of membrane-associated proteins in the process and imply a mechanism that coordinates autonomous behaviors of individual cells within epithelial structures.