Hybridization often occurs at the parapatric range interface between closely related species, but fitness outcomes vary: hybrid offspring exhibit diverse rates of viability and reproduction when compared to their parental species. The mobile hybrid zone between two chickadee congeners ( Poecile atricapillus x P. carolinensis ) has been well studied behaviorally and genetically but the viability of hybrids, as well as the underlying mechanisms contributing to hybrid fitness, have remained unclear. To better characterize the fitness costs of hybridization in this system, we analyzed 21 years of data from four sites, including over 1,400 breeding attempts by the two species, to show that rates of hatching success changed substantially as the zone of hybridization moved across the landscape. Admixture-associated declines in hatching success correlated with reduced proportions of heterogametic (female) offspring as predicted by Haldane’s rule. Our data support an underlying mechanism implicating genetic admixture of the homogametic (male) parent as the primary determinant of offspring sex ratio, via incompatibilities on the hemizygous Z chromosome. Our long-term study is the first to directly measure changes in fitness costs as a vertebrate hybrid zone moves, and it shows that changes in these costs are a way to track the distribution of a hybrid zone across the landscape.