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Powdery mildew (PM) is a common fungal disease in many important crops. The PM caused by Podosphaera xanthii has been the most challenging problem in commercial Gerbera (Gerbera hybrida) production globally, often leading to severe losses of crop yield and quality. A small number of PM-resistant breeding lines and cultivars have been reported in Gerbera, but the underlying genetics for PM resistance in Gerbera is largely unknown. Scarcity of genomic resources such as genetic linkage maps and molecular markers has severely hindered the effort to understand the genetic basis and locate loci controlling PM resistance in Gerbera. This study aimed to construct a genome-wide genetic linkage map, identify quantitative trait loci (QTL), and molecular markers for PM resistance in Gerbera. A segregating mapping population was developed by crossing PM-resistant and -susceptible Gerbera breeding lines, genotyped by sequencing, and phenotyped for PM resistance. A genome-wide genetic linkage map constructed with 791 single polymorphic site (SNP) markers spans 1912.30 cM across 27 linkage groups (LG) and reaches a density of 1 marker per 2.42 cM. One major consistent QTL was discovered in LG16, explaining more than 16.6% of the phenotypic variance for PM resistance. The QTL was tagged with two flanking SNP markers. The availability of this genetic linkage map will be very useful for locating and tagging QTLs for other important traits in Gerbera, and the newly discovered QTL and SNP markers will enable development of molecular markers for improving Gerbera for resistance to PM.