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Despite repeated shifts in virulence, contrasting reproductive histories, and emerging fungicide insensitivity, the genomic basis of its diversification and adaptation remains poorly understood.\n                        <\/jats:p>\n                      <\/jats:list-item>\n                      <jats:list-item>\n                        <jats:p>\n                          In this study, we generated haplotype\u2010resolved, chromosome\u2010level genome assemblies for two isolates with contrasting virulence and analyzed 41 Australian isolates collected over 54\u2009yr (1966\u20132020), integrating comparative and population genomics, mating\u2010type gene phylogenies, chromosome\u2010specific\n                          <jats:italic>k<\/jats:italic>\n                          \u2010mer profiling, genome\u2010wide copy\u2010number variation (CNV) analysis, and gene\u2010expression analysis.\n                        <\/jats:p>\n                      <\/jats:list-item>\n                      <jats:list-item>\n                        <jats:p>\n                          We identified a structurally dynamic chromosome characterized by repeat\u2010associated rearrangements, structural variation, and lineage\u2010associated CNV, representing the first evidence in a rust fungus of chromosome\u2010scale structural diversification of this extent. Population analyses distinguished clonally expanded lineages from recombination\u2010associated lineages, with mating\u2010type gene phylogenies providing further support for lineage differentiation. More recently collected isolates showed increased duplication\u2010associated variation, and CNV boundaries were associated with structural\u2010variant breakpoints. We also identified lineage\u2010associated amplification of\n                          <jats:italic>Cyp51<\/jats:italic>\n                          , with increased copy number associated with higher transcript abundance, supporting a potential role in fungicide adaptation.\n                        <\/jats:p>\n                      <\/jats:list-item>\n                      <jats:list-item>\n                        <jats:p>\n                          Overall, our findings highlight structural variation, contrasting reproductive histories, and lineage\u2010associated CNV as important contributors to diversification in\n                          <jats:italic>P. hordei<\/jats:italic>\n                          , providing insights for future rust pathogen surveillance and management strategies.\n                        <\/jats:p>\n                      <\/jats:list-item>\n                    <\/jats:list>\n                  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