Abstract Balancing selection is a form of natural selection maintaining diversity at the sites it targets and at linked nucleotide sites. It is generally expected to facilitate the accumulation of a “sheltered” genetic load of linked deleterious mutations, but the overall extent of its genomic impact remains poorly documented. Taking advantage of plant self-incompatibility as one of the best-understood and most intense examples of long-term balancing selection, we provide the most highly resolved picture of the effect of balancing selection on the sheltered genetic load in any plant genome. We used targeted genome resequencing to evaluate the intensity of indirect selection on the genomic region flanking the self-incompatibility locus in three sample sets in each of the two closely related plant species Arabidopsis halleri and A. lyrata , and used 100 control regions from throughout the genome to factor out differences in demographic histories and/or sample structure. Nucleotide polymorphism increased strongly around the S -locus in all sample sets, but only over a limited genomic extent, as it became indistinguishable from the genomic background beyond the first 25kb. Genes around the S -locus carried more mutations than those in the control regions, but in contrast to the classical model for the accumulation of the sheltered load we observed no relaxation of the efficacy of purifying selection. Overall, our results challenge our understanding of how natural selection in one genomic region affects the evolution of the adjacent genomic regions, and have consequences for how systems of mating that enforce outcrossing in populations are maintained.