Feathers are complex epidermal organs and remarkable evolutionary innovations, but the signals that specify their identity are poorly understood. Classical grafting experiments in the 1950s had indicated that chicken feather identity was specified early in wing development. Now Maria Ros, Matthew Towers and colleagues discover a role for Sonic hedgehog (Shh) signalling, derived from the polarising region and acting in a paracrine manner, in flight feather specification. Inhibition of Shh signalling at the earliest stages of chick wing development leads to the later loss of flight feather buds, and only down feather buds remain that make no ligamentous connections to the skeleton. The comparison of transcriptomes of tissues fated to form flight feathers (posterior border of normal wings and feather-bearing legs of Pekin bantams) and not forming flight feathers (normal wing after Shh inhibition and normal chick leg) identifies several transcription factors, including the flight feather marker Sim1, as lost or reduced following early Shh inhibition. Loss- and gain-of-Shh function, by time-specific abolition or polarising region grafting experiments, reveals that Shh specifies later Sim1 expression in a defined spatiotemporal sequence (similar to how it regulates digit identity in wings and legs). Finally, Shh inhibition results in the failure of flight feather formation in hatchlings and mature birds. This work suggests that birds co-opted the existing, Shh-dependent, positional information digit patterning mechanism for feather development.