The remarkable architecture of their respiratory system enables the unique metabolic performance that makes insects so successful. We performed single-cell RNAseq analysis of the larval tracheal system of Drosophila melanogaster and identified 17 cell populations that are part of or closely associated with the trachea. In addition to several groups of epithelial cells and different progenitor cell types, the secretory Inka cells showed unexpected properties. These cells express almost all the molecular elements of the presynaptic active zone and the neurotransmitter vesicle release machinery, both characteristic features of neurons. Some of these molecular elements are essential for their secretory function. In addition, we could molecularly map the different progenitor cell types and their different developmental stages. The data collected in this work represents a valuable resource for future studies focusing on this critical organ. The most important finding of this study is that Inka cells have neuron-like properties, which challenges the traditional picture of the distinction between neuronal and non-neuronal cells.