Abstract Self-incompatibility in flowering plants is a common mechanism that prevents self-fertilization and promotes outcrossing. In Brassicaceae, there is high genetic diversity at the locus controlling self-incompatibility, and dozens of distinct alleles are organized in a complex dominance hierarchy: the gene controlling self-incompatibility specificity in pollen shows monoallelic expression in heterozygote individuals. This is achieved through the action of sRNA precursors that resemble miRNAs, although the underlying molecular mechanisms remain elusive. Here, we engineered Arabidopsis thaliana lines expressing components of the Arabidopsis halleri self-incompatibility system, and used a reverse genetics approach to pinpoint the pathways underlying the function of these sRNA precursors. We showed that they trigger a robust decrease in transcript abundance of the recessive pollen self-incompatibility genes, but not through the canonical transcriptional or post-transcriptional gene silencing pathways. Furthermore, we observed that single sRNA precursors are typically processed into hundreds of sRNA molecules of distinct sizes, abundance levels and ARGONAUTE loading preferences. This heterogeneity closely resembles that of proto-miRNAs, the evolutionary ancestors of miRNAs. Our results suggest that these apparently arbitrary features, which are often associated with lack of effects on gene expression, are crucial in the context of the self-incompatibility dominance hierarchy since they allow for one sRNA precursor of a given allele to repress multiple other recessive alleles. This study not only provides an in-depth characterization of the molecular features underlying complex dominance interactions, but also constitutes a unique example of how specific evolutionary constraints shape the progression of sRNA precursors along the proto-miRNA - miRNA evolutionary continuum. Significance statement miRNAs are genetically encoded small non-coding RNA molecules that control gene expression. Here, we characterized a set of regulatory loci present in the self-incompatibility locus of Arabidopsis halleri which resemble proto-miRNAs, the evolutionary ancestors of miRNAs. We report that despite the absence of classical miRNA features thought to be essential for gene expression regulation, proto miRNAs generated by these loci robustly repress the activity of self-incompatibility genes through non canonical silencing pathways, and thus function to establish a complex dominance hierarchy between self-incompatibility alleles. We show that the evolutionary forces promoting diversity of self incompatibility alleles have likely favored the maintenance of proto-miRNA features in order to mediate dominance interactions between numerous alleles, thus preventing the transition of self-incompatibility proto-miRNAs into canonical miRNAs.