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We used whole-genome sequencing to analyse a collection of 35 fluconazole resistant and 7 susceptible isolates together with coverage analysis and GWAS techniques to identify new mechanisms of fluconazole resistance. Phylogenetic analysis shows that although the collection is diverse, two probable outbreak groups were identified. We identified copy number variation of two genes, and , in resistant isolates. Two strains have a CNV at the locus; the entire ORF is amplified in one, and only the promoter region is amplified in the other. We show the annotated telomeric gene is actually an artefactual fusion of two highly similar neighbouring genes due to an assembly error in the CDC317 reference genome. We report highly variable copy numbers of the region across the collection. Several strains have increased expansion of the two genes into a tandem array of new chimeric genes. Other strains have experienced a deletion between the two genes creating a single gene with a reciprocal chimerism. We find translocations, duplications, and gene conversion across the gene family in the species complex, showing that it is a highly dynamic family.