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Summary Self‐incompatibility alleles (S‐alleles), which prevent self‐fertilisation in plants, have historically been expected to benefit from negative frequency‐dependent selection and invade when introduced to a new population through gene flow. However, the most taxonomically widespread form of self‐incompatibility, the ribonuclease‐based system ancestral to the core eudicots, functions through collaborative non‐self recognition, which can affect both short‐term patterns of gene flow and the long‐term process of S‐allele diversification.We analysed a model of S‐allele evolution in two populations connected by migration, focussing on comparisons among the fates of S‐alleles initially unique to each population and those shared among populations.We found that both shared and unique S‐alleles from the population with more unique S‐alleles were usually fitter compared with S‐alleles from the population with fewer S‐alleles. Resident S‐alleles often became extinct and were replaced by migrant S‐alleles, although this outcome could be averted by pollen limitation or biased migration.Collaborative non‐self recognition will usually either result in the whole‐sale replacement of S‐alleles from one population with those from another or else disfavour introgression of S‐alleles altogether.