Sexual selection operates via female choice and male competition, which can act independently, in concert, or in opposition. Female choice is typically considered the stronger selective force, but how these two processes interact to shape phenotypic divergence is poorly understood. I tested the hypothesis that variation in sexual selection in different habitats drives song divergence in the greenish warbler ring species. I evaluated the strength, direction, and targets of female choice and male competition in three populations spanning 2400km of latitude. Average song length increased with latitude, concomitant with a decline in population density. Within populations, males sang longer songs when females were fertile and shorter songs during territory establishment. Females consistently preferred males with longer songs and larger song repertoires. By contrast, playback experiments showed that males used short songs in territory defense. Songs were shortest at high densities, and in the highest density population only, song traits preferred by females correlated with male territoriality. Stronger male competition at high population densities likely constrains maximum song length, whereas weaker competition at low densities allows expression of female choice for long songs. Interactions between male competition and ecology may be a crucial but oft-overlooked component of phenotypic divergence and speciation.