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Abstract Hybridization and introgression are widespread in nature, with important implications for adaptation and speciation. Since heterogametic hybrids often have lower fitness than homogametic individuals, a phenomenon known as Haldane’s rule, loci inherited strictly through the heterogametic sex rarely introgress. We focus on the Y-chromosomal history of guenons, African primates that hybridized extensively in the past. Although our inferences suggest that Haldane’s rule generally applies, we uncover a Y chromosome introgression event between two species ca. six million years after their initial divergence. Using simulations, we show that selection likely drove the introgressing Y chromosome to fixation from a low initial frequency. We identify non-synonymous substitutions on the novel Y chromosome as candidate targets of selection, and explore meiotic drive as an alternative mechanism. Our results provide a rare example of Y chromosome introgression, showing that the ability to produce fertile heterogametic hybrids likely persisted for six million years in guenons.