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Summary Mate limitation in small populations can reduce reproductive fitness, hinder population growth, and increase extinction risk. Mate limitation is exacerbated in self‐incompatible (SI) taxa, where shared S‐alleles further restrict mating. Theory suggests genetic drift as a predictor of mate limitation and the breakdown of SI systems. We tested this prediction by evaluating mate availability and S‐allele number in populations of a tetraploid herb with gametophytic SI (GSI) spanning a range of effective population sizes. We performed controlled crosses in 13 populations of Argentina anserina to quantify mate availability and S‐allele diversity, which were compared with simulations of tetraploid populations with GSI. We further evaluated mechanisms at the pollen–pistil interface contributing to outcross failure and leakiness in self‐recognition. Mate availability declined in small populations, and closely fit tetraploid GSI population genetic models where maternal plants receive pollen with diverse S‐alleles generated through tetrasomic inheritance. The failure to arrest self‐pollen in the style was common in some populations. Specifically, leaky SI was more common in small populations with low mate availability, where it explained higher seed production in natural populations. The restriction of leaky self‐recognition to the smallest populations is consistent with mate limitation as a pressure driving the breakdown of self‐incompatibility. [ABSTRACT FROM AUTHOR]