Cilia are specialized structures found on a variety of mammalian cells, with variable roles in the transduction of mechanical and biological signals (by primary cilia, PC), as well as in the generation of fluid flow (by motile cilia). Their critical role in the establishment of a left-right axis in early development is well described, as well as in the defense immune function of multiciliated upper airway epithelium. By contrast, detailed analysis of the ciliary status of specific cell types during organogenesis and postnatal development has received less attention. In this study, we investigate the progression of ciliary status within the endothelium and mesenchyme of the lung. Remarkably, we find that pulmonary endothelial cells (ECs) lack PC at all stages of development, except in low numbers in the proximal portions of older pulmonary arteries. Mesenchymal cells, by contrast, widely exhibit PC in early development, and a large subset of PDGFRα+ fibroblasts maintain PC into adulthood. The dynamic and differential ciliation of multiple cellular populations in the developing lung both challenges prior assertions that PC are found on all cells and highlights a need to understand their spatiotemporal functions.