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The variability of intron density among eukaryotes is puzzling and still debated. Most previous studies have been limited because of the near absence of intron presence–absence polymorphism (IPAP) within species or because comparisons could be made only between distantly related species. We conducted population genetic analyses on eight loci showing IPAP to investigate the effect of natural selection on intron dynamics in a global collection of the panmictic fungal plant pathogen Zymoseptoria tritici and its very close relatives. Five of these loci likely represent recent intron gains because their absence is fixed among the closest relatives of Z. tritici, and three likely represent recent intron losses because their presence is fixed among the close relatives. We analyzed signatures of selection by comparing allele frequencies, nucleotide diversities, and rates of recombination and found compelling evidence that at least two out of the five intron-gain loci, a SWIM zinc-finger gene and a sugar transporter, are under directional selection favoring alleles that gained the intron. Our results suggest that the intron-present alleles of these loci are sweeping to fixation, providing a genetic hitchhiking mechanism to explain rapid intron gain in Z. tritici. The overall findings are consistent with the hypothesis that intron gains are more likely to be driven by selection while intron losses are more likely to be due to neutral processes such as genetic drift.