Recombination suppression often evolves in sex chromosomes and around mating-type loci. In the invasive chestnut blight fungus Cryphonectria parasitica (Ascomycota), a genomic region was previously suggested to lack recombination and to be partially linked to the mating-type (MAT) locus based on the analysis of a few progenies. Using hundreds of available C. parasitica genomes and generating several new high-quality genome assemblies from the native and introduced range of the pathogen, we show that a ca. 1.2 Mb genomic region proximal to the mating-type locus lacks recombination worldwide. In invasive populations, this MAT-proximal region displayed two highly differentiated haplotypes, that were strongly associated to mating types, but not completely. High-quality assemblies revealed an inversion in one of the haplotypes and footprints of degeneration worldwide, the MAT-proximal region being enriched in gene disruptions, non-synonymous substitutions and transposable elements in both haplotypes. The divergence between the two haplotypes was estimated to have occurred at least 1.5 million years ago and two haplotypes segregate in all continents, including the native range. High differentiation between haplotypes, their occurrence on different continents, their balanced frequencies within populations, their genomic rearrangements and degeneration worldwide, altogether suggest an ancient recombination suppression maintained by selection. The MAT-Proximal region carries multiple genes upregulated under virus infection or vegetative incompatibility reaction. This study sheds light on a case of a large non-recombining region partially linked to a mating compatibility locus, and on balancing selection maintaining differentiated haplotypes, possibly involving deleterious mutations and/or host or virus adaptation in a devastating tree pathogen.