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Description: In many species, including primates, cetaceans, and birds, individuals learn population-specific cultural traits such as song or contact vocalizations from social interactions with their parents or with other group members. Although cultural traits can be ecologically relevant for individuals and populations, the evolutionary significance of animal culture is less clear. Recent studies proposed that culture shapes population genetic structure and diversity, but the role of culture as a mechanism for reproductive isolation and as a potential driver of speciation remains controversial. Here, we show that variation in socially-learnt song, rather than differences in inherited, morphological traits, results in strong assortative mating in zebra finches (Taeniopygia guttata). We studied mating patterns across three consecutive generations using captive populations that have evolved in isolation for about 100 generations and that differ substantially in body size. Cross-fostering eggs within and between these morphologically and culturally distinct populations, and quantifying social interactions of the resulting offspring, revealed that mate choice targets cultural traits that are transmitted during a short developmental window. Pair formation was independent of body size, but individuals mated assortatively for the type of song their parents once learnt from their foster-parents. Our study solves the classical nature versus nurture debate for both the mating preferences and the phenotypic traits on which these preferences are focused. Our results demonstrate that social learning during early life can have profound consequences for mate choice and suggest that cultural traits can contribute to reproductive isolation.