Color divergence is increasingly recognized as important for speciation in songbirds through its influence on social dynamics. However, the behavioral mechanisms underlying the eco-evolutionary feedback that acts across species boundaries is poorly understood. The hybrid zone between Setophaga occidentalis (SOCC) and S. townsendi (STOW) in the Cascade mountain ranges provides a natural observatory to test the interplay between genetics and social behaviour in maintaining species boundaries. Recently, we found that selection within a gene block underpinning color variation (ASIP-RALY) has maintained a stable and narrow hybrid zone. Here we investigated the social signaling roles of cheek darkness and flank streaking, two color traits linked to ASIP-RALY that reflect opposing dominance of SOCC and STOW alleles. We found that both traits act as honest badges of status, as they predicted male breeding quality. The opposing dominance effects of ASIP-RALY resulted in signal discordance for heterozygotes, which in turn was associated with inferior hybrid territorial performance, a fitness proxy quantified by vocal and physical responses of resident males to a decoy intruder. Taken together, this study highlights a potential behavioral mechanism underlying selection acting on a simple genetic architecture that has maintained a stable species boundary over decades despite significant gene flow.