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Influential models of speciation by sexual selection posit either a single shared preference for a universal display, expressed only when males are locally adapted and hence in high condition, or that shared loci evolve population-specific alleles for displays and preferences. However, many closely related species instead show substantial differences across categorically different traits. We present a model of secondary contact whereby females maintain preferences for distinct displays that indicate both male condition and their match to distinct environments, fostering reproductive isolation among diverging species. This occurs even with search costs and with independent preference loci targeting independent displays. Such preferences can also evolve from standing variation. Divergence occurs because condition-dependent display and female preference depend on local ecology, and females obtain different benefits of choice. Given the ubiquity of ecological differences among environments, our model could help explain the evolution of striking radiations of displays seen in nature.