We carried out two experiments across 2 yr on song perception in female cowbirds (Molothrus ater). In the first experiment, juvenile and adult female brown-headed cowbirds, living in same-sex flocks in outdoor aviaries, were periodically tutored with recordings of local male cowbirds’ songs. In the spring, four adult male cowbirds were placed with half of the females for a 12-d period. We then tested song preferences of all females by measuring copulation solicitation displays during the breeding season. We found that the females exposed only to tape-tutor songs preferred those songs to those of the unfamiliar males used as companions and that the females allowed to interact with males preferred their songs over the familiar tape-tutor songs. These data establish the modifiability of female cowbirds’ song preferences at the level of local song. In a second experiment, we studied the playback responses of juvenile females, hand-reared from the egg, who were tape-tutored only in the spring in the presence or absence of adult females. There were no differences between the responses of juveniles housed with or without adult females and the hand-reared juveniles were significantly less responsive to song than adult females. Adult females responded more to familiar songs than to the unfamiliar songs: juvenile females made no such distinction. Taken as a whole, these data are the first to document that female cowbirds’ song preferences for local song can be reshaped by post-natal experience. These data complement recent study in cowbirds and other species showing that socially more complex contexts reveal plasticity in female song preferences that are not apparent when learning opportunities are constrained by impoverished laboratory settings.