<p>Birdsong has historically been characterized as a sexually selected, primarily male behaviour. Recent findings suggest that female song is widespread, raising questions about how social functions of birdsong shape song evolution. Certain social behaviours, such as cooperative breeding, could alter selection pressures on both sexes and potentially influence the evolution of both female and male song. Here we use phylogenetic comparative analyses across 1,041 songbird species to examine relationships between cooperative breeding, female song and male song characteristics. We show robust bidirectional coevolutionary dynamics between cooperative breeding and female song that persist when controlling for territoriality, allometry, phylogenetic uncertainty, geographical sampling and analytical biases. While cooperative breeding and female song commonly co-occur in strongly territorial systems, their association is especially pronounced in weakly territorial systems, where they co-occur much more often than expected by chance. Additionally, we observe that male song repertoire size evolves more slowly in cooperative breeding lineages. These findings demonstrate that cooperative breeding shapes the evolution of vocal communication differently based on territorial context and sex, with female song potentially serving crucial but understudied functions related to social cohesion in cooperative systems, particularly in species where territorial conflict is reduced.</p>