The dorsal air sacs supply oxygen to the flight muscles of the Drosophila adult. This tracheal organ grows from an epithelial tube (the air sac primordium (ASP)) that arises during the third larval instar (L3) from a wing-disc-associated tracheal branch. Since the ASP is generated by a program of both morphogenesis and cell proliferation and since the larval tracheal branches are populated by cells that are terminally differentiated, the provenance of its progenitors has been uncertain. Here, we show that, although other larval tracheae are remodeled after L3, most tracheal branches in the tracheal metamere associated with the wing disc (Tr2) are precociously repopulated with imaginal tracheoblasts during L3. Concurrently, the larval cells in Tr2 undergo head involution defective (hid)-dependent programmed cell death. In BX-C mutant larvae, the tracheal branches of the Tr3 metamere are also repopulated during L3. Our results show that repopulation of the larval trachea is a prerequisite for FGF-dependent induction of cell proliferation and tubulogenesis in the ASP and that homeotic selector gene function is necessary for the temporal and spatial control of tracheal repopulation.