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The evolution of flight in feathered dinosaurs and early birds over millions of years required flight feathers whose architecture features hierarchical branches. While barb-based feather forms were investigated, feather shafts and vanes are understudied. Here, we take a multi-disciplinary approach to study their molecular control and bio-architectural organizations. In rachidial ridges, epidermal progenitors generate cortex and medullary keratinocytes, guided by Bmp and transforming growth factor β (TGF-β) signaling that convert rachides into adaptable bilayer composite beams. In barb ridges, epidermal progenitors generate cylindrical, plate-, or hooklet-shaped barbule cells that form fluffy branches or pennaceous vanes, mediated by asymmetric cell junction and keratin expression. Transcriptome analyses and functional studies show anterior-posterior Wnt2b signaling within the dermal papilla controls barbule cell fates with spatiotemporal collinearity. Quantitative bio-physical analyses of feathers from birds with different flight characteristics and feathers in Burmese amber reveal how multi-dimensional functionality can be achieved and may inspire future composite material designs. • A cortex/medulla composite beam organization allows rachides to adapt flexibly • Polarized adhesion and keratin expression lead to hooklet barbules that form vanes • With-dermal papilla WNT signaling controls barbule shape along the feather P-D axis • 3D feathers embedded in amber show primitive vanes formed by overlapping barbules The design and developmental paradigms of flight feathers are explored using a combination of bio-physical analyses, molecular characterization, and evolutionary comparisons across a broad range of birds with different flight modes, revealing a modular architectural design that can accommodate diverse eco-spaces. [ABSTRACT FROM AUTHOR]