Color is a phenotypic trait of particular significance to birds, which are known for their diverse color signals and color-producing mechanisms including pigments, light scattering from nanostructured feather tissues and combinations of the two. Hummingbirds are a highly diversified lineage with bright, iridescent plumage colors. The physical bases of this bright coloration are the arrays of hollow, melanin-containing platelets (melanosomes) within feather barbules that produce color through multilayer interference. Almost nothing is known of either how these unusual melanosomes form or of how they are arranged into highly organized nanostructures. Such knowledge is critical to understand their evolution and may provide inspiration for new synthetic optically active materials. Here, we assembled a developmental time series of growing feathers and used optical and electron microscopy to determine the sequential steps of platelet development and self-assembly into organized layers. We show that hummingbird platelets contain air bubbles early in their development inside melanocytes and, surprisingly, expand up to four times their initial size before completion of development. Organization occurs through apparently passive mechanisms driven by the high density of melanosomes inside the highly flattened barbules. Three-dimensional reconstructions using electron tomography affirm the precise organization of these fully developed nanostructures. Our data, in conjunction with data from other species, suggest that diverse developmental pathways guide the production of highly derived pigment organelles and the nanostructures they create.