Identifying the genes underlying adaptation, their distribution in genomes and the evolutionary forces shaping genomic diversity are key challenges in evolutionary biology. Very few studies have investigated the abundance and distribution of selective sweeps in species with high-quality reference genomes, outside a handful of model species. Pathogenic fungi are tractable eukaryote models for investigating the genomics of adaptation. By sequencing 53 genomes of two species of anther-smut fungi and mapping them against a high-quality reference genome, we showed that selective sweeps were abundant and scattered throughout the genome in one species, affecting near 17% of the genome, but much less numerous and in different genomic regions in its sister species , where they left footprints in only 1% of the genome. Polymorphism was negatively correlated with linkage disequilibrium levels in the genomes, consistent with recurrent positive and/or background selection. Differential expression in planta and in vitro, and functional annotation, suggested that many of the selective sweeps were probably involved in adaptation to the host plant. Examples include glycoside hydrolases, pectin lyases and an extracellular membrane protein with CFEM domain. This study thus provides candidate genes for being involved in plant–pathogen interaction (effectors), which have remained elusive for long in this otherwise well-studied system. Their identification will foster future functional and evolutionary studies, in the plant and in the anther-smut pathogens, being model species of natural plant–pathogen associations. In addition, our results suggest that positive selection can have a pervasive impact in shaping genomic variability in pathogens and selfing species, broadening our knowledge of the occurrence and frequency of selective events in natural populations.