Female song is widespread, and likely ancestral. However, we currently know relatively little about when and why females sing, or what the fitness consequences might be for individual differences in song rates. Female song might function in female-male communication, or in the context of female-female competition for reproductive resources. In either case, song rates may be related to reproductive success. However, changes in resource availability may alter contest rules and the relationship between song rates and reproductive success. To address these questions, we quantified female song patterns across breeding stage, and determine how female song rates relate to reproductive success, in two populations of superb fairy-wrens (Malurus cyaneus) that differ in habitat quality and population density. Female song rates were highly repeatable across date and stage, and females sang more frequently than males in response to playback of novel female song, but breeding stage had no effect on song rates in either sex. Further, we observed a marked population difference in female song rates, and in the relationship between song rates and reproductive success. Females in high quality habitat sang less frequently overall, but females that sang more in response to playback had greater reproductive success. In contrast, females in low quality habitat sang more frequently, but females that sang most occupied poor quality territories and had reduced reproductive success. Together, these results indicate a strong role for female-female competition for resources rather than communication with males. The context dependent relationship between song and fitness suggests that female song is an potential target for selection, but that resource availability can alter female contest rules and shape how selection acts on female song.