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Female mating preferences for exaggerated male display traits are commonplace. Yet, comprehensive understanding of the evolution and persistence of costly female preference through indirect (Fisherian) selection in finite populations requires some explanation for the persistence of additive genetic variance (Va) underlying sexual traits, given that directional preference is expected to deplete Va in display and hence halt preference evolution. However, the degree to which Va, and hence preference‐display coevolution, may be prolonged by spatially variable sexual selection arising solely from limited gene flow and genetic drift within spatially structured populations has not been examined. Our genetically and spatially explicit model shows that spatial population structure arising in an ecologically homogeneous environment can facilitate evolution and long‐term persistence of costly preference given small subpopulations and low dispersal probabilities. Here, genetic drift initially creates spatial variation in female preference, leading to persistence of Va in display through "migration‐bias" of genotypes maladapted to emerging local sexual selection, thus fueling coevolution of costly preference and display. However, costs of sexual selection increased the probability of subpopulation extinction, limiting persistence of high preference‐display genotypes. Understanding long‐term dynamics of sexual selection systems therefore requires joint consideration of coevolution of sexual traits and metapopulation dynamics. [ABSTRACT FROM AUTHOR]