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Abstract Feathers are complex structures exhibiting structural/functional disparity across species and plumage. Flight was lost in >30 extant lineages from ~79.58 Ma–15 Ka. Effects of flight loss on senses, neuroanatomy, and skeletomusculature are known. To study how flightlessness affects feathers, we measured 11 feather metrics across the plumage of 30 flightless taxa and their phylogenetically closest volant taxa, with broader sampling of primaries across all orders of crown birds. Our sample includes 27 independent flight losses, representing nearly half of extant flightless species. Feather asymmetry measured by barb angle differences between trailing and leading vanes decreases in flightless lineages, most prominently in flight feathers and weakest in contour feathers. Greatest changes in feather anatomy occur in older flightless lineages (penguins, ratites). Comparative methods show that many microscopic feather traits are not dramatically modified after flightlessness compared to body mass increase and relative wing and tail fan reduction. Changes involved with greater vane symmetry show stronger shifts, however. Relaxing selection for flight does not rapidly modify feather flight adaptations, apart from asymmetry. Developmental constraints and relaxed selection for novel feather morphologies may explain some observed changes. Macroscopic changes to flight apparati (skeletomusculature, airfoil size) are more evident in recently flightless taxa and could more reliably detect flightlessness in fossils, with increased feather symmetry as a potential microscopic signal. We observed apical modification in later stages of feather development (asymmetric displacement of barb loci), while morphologies arising during early developmental stages are only altered after millions of years of flightlessness.