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Long-read genomics reveal extensive nuclear-specific evolution and allele-specific expression in dikaryotic wheat stripe rust fungus Phased telomere-to-telomere (T2T) genome assemblies are transforming our understanding of complex genome features such as centromeres, rDNA repeats, and allele-specific expression (ASE). However, insights into dikaryotic fungi, which maintain separate haploid nuclei, remain limited. This study investigates the genome biology of a long-term asexual clone of the wheat pathogenic fungus Puccinia striiformis f. sp. tritici. Using Oxford Nanopore duplex sequencing and Hi-C, a highly accurate T2T nuclear-phased assembly was generated. The fungus exhibits large centromeres enriched in retrotransposons, with single kinetochore attachment sites per chromosome. Centromeric regions between haploid genomes are highly diverse and lack positional conservation. Each nucleus has a unique array of rDNA sequences with extensive variation. Structural variations driven by transposable elements contribute to inter-haplotype diversity. Long-read cDNA analysis revealed ASE in nearly 20% of heterozygous genes, particularly infection-related genes, linked to CpG methylation. This suggests epigenetic ASE regulation plays a key role in fungal virulence. This study sheds new light into the genome biology and adaptive evolutionary potential of rust fungi, with important implications for managing their agricultural impacts.