In ecological evolutionary developmental biology (Eco‐Evo‐Dev), one aspires to decipher the interaction principles among an organism’s environment, genes, and development, across an individual’s life span or evolutionary scales. Animal integuments form the interface between an organism and its environment, have to adapt to dynamic environmental changes, and changes are apparent for our investigation; therefore, the integument becomes a great model for Eco‐Evo‐Devo study. Among the integuments, feathers offer an opportunity to examine aspects of evolution which began in feathered dinosaurs and early birds about 150 million years ago. These studies enable us to decipher the mechanisms of how a skin appendage evolve from endothermy function to communication to flight, becoming a highly complex and functional integumentary organ. The transformation from scales to feathers required the formation of multiple periodically arranged growth units. The conversion of each feather primordium into a follicle with epidermal stem cells and dermal papilla niche allows cyclic renewal of the feather structures and potential to generate new phenotypes. The feather is made of two modules: a central shaft (rachis) and peripheral branches (barbs), both are modifiable genetically and epigenetically. The hierarchical feather filament branches allow endless combinations of functional feather forms. Follicular pigment stem cells work with structure and chemical coloring mechanisms to generate complex color patterns on feather vane for communication. Here we take a multi‐disciplinary approach to study the molecular control and bio‐architectural principles used to construct a flight feather. Developmental studies show the rachis is made of the cortex and medulla, and medulla is defective in chicken frizzle mutants which exhibit curly feathers. The differentiation of cortex and medulla from epidermal progenitors is controlled by Bmp and TGFβ signaling, leading to bilayer composite beams with unique topological arrangement and biophysical properties. Within barb ridges, epidermal progenitors generate cylindrical, plate or hooklet‐shaped barbule cells that form fluffy branches for endothermy or feather vanes for air‐flapping, mediated by asymmetric cell junctions and keratin expression. Transcriptome analyses and functional studies show anterior‐posterior Wnt2b signaling within the dermal papilla controls barbule cell fates with spatial‐temporal collinearity. Retinoic acid and Gremlin mediate medio‐lateral asymmetric vane formation, a feature critical for the aero‐engineering of flight. Quantitative bio‐physical analyses of flight feathers from birds with diverse flight characteristics, ranging from ostriches, chickens, eagles, finches, to hummingbirds and penguins show how flight feathers can be light and strong at the same time and adapt to different environmental needs robustly. Finally, feathers embedded in Burmese amber 99 million years ago allows 3D analyses of ancient feather forms. Together, the results show how multi‐dimensional functionalities are achieved by modifying a prototypic core feather morphogenetic module, which enables the birds to venture into new eco‐spaces. The new findings can also inspire future composite material designs.