The thermotolerant multidrug-resistant ascomycete Candida auris rapidly emerged since 2009 and simultaneously evolved in different geographical zones worldwide, causing superficial as well as systemic infections . The molecular events that orchestrated this sudden emergence of the killer fungus remain mostly elusive . Here, we identify centromeres in C. auris and related species, using a combined approach of chromatin immunoprecipitation and comparative genomic analyses . We find that C. auris and multiple other species in the Clavispora/Candida clade shared a conserved small regional centromere landscape lacking pericentromeres . Further, a centromere inactivation event led to karyotypic alterations in this species complex . Inter-species genome analysis identified several structural chromosomal changes around centromeres . In addition, centromeres are found to be rapidly evolving loci among the different geographical clades of the same species of C. auris . Finally, we reveal an evolutionary trajectory of the unique karyotype associated with clade 2 that consists of the drug susceptible isolates of C. auris.