The present ultrastructural and immunocytochemical study on the embryonic feathers of the zebrafinch, an altricial passerine bird, describes cellular differentiation of developing downfeathers. Barb ridges are folds of the original epidermis of the embryonic feather germ in which the basal–apical polarity of epidermal cells is upset. The result is the loss of most germinal activity of basal cells of the barb ridges so that only the embryonic epidermal layers remain. The more external layer is the primary periderm, followed by 4–6 layers of inner-periderm cells that mature into feather sheath and barb vane ridge cells. The following layer, the subperiderm, produces a small type of beta-keratin typical of feathers. In barb ridges, the subperiderm layer is displaced to form barbule plates and barb cells. The formation of branching barbules occurs by the presence of barb vane ridge cells that function as spacers between barbule cells. The fourth layer is homologous to the germinal layer of the epidermis, but in barb ridges it rapidly loses the germinal capability and becomes the cyclindrical layer of marginal plates. The study indicates that a necrotic process determines the carving out of the final feather shape, although apoptosis may also play a role. In fact, after barb and barbule cells have formed a keratinized syncitium, retraction of the vascular bed determines anoxia with the resultant necrosis of all feather cells. Only those of the keratinized syncitium remain to form the feather while supportive cells disappear. The sheath covering the barb and barbule syncitium is lost by the formation of a sloughing layer following degeneration of external barb ridge vane cells and loss of the sheath. It is proposed that the evolution of the morphogenetic process of barb ridge formation was peculiar to tubular outgrowths of the integument of archosaurian reptiles that evolved into birds. Once established in the embryonic programmes of skin morphogenesis of ancient birds, variations in the process of barb ridge morphogenesis allowed the fusion of ridges into large or branched ridges that originated the rachis. This process produced pennaceous feathers, among which were those later used for flight. The present study stresses that the morphogenetic process of barb ridge formation determines the concomitant appearance of barbs and barbules. As a consequence, intermediate forms of evolving feathers with only barbs but not barbules are unlikely or are derived from alteration of the above basic morphogenetic mechanism.