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Chrysomyxa rusts are fungal pathogens widely present in the boreal forest. Taxonomic delimitation and precise species identification are difficult within this genus since several species display similar morphological features. We applied a DNA barcode system based on the ribosomal internal transcribed spacer region (ITS), large subunit (28S) ribosomal RNA gene, mitochondrial cytochrome oxidase 1 (CO1) and mitochondrial NADH dehydrogenase subunit 6 (NAD6) in 86 strains from 16 different Chrysomyxa species, including members of the Chrysomyxa ledi species complex. The nuclear ITS and 28S loci revealed higher resolving power than the mitochondrial genes. Amplification of the full CO1 barcode region failed due to the presence of introns limiting the data set obtained with this barcode. In most cases, the ITS barcodes were in agreement with taxonomic species based on phenotypic characters. Nevertheless, we observed genetically distinct (different DNA barcodes) lineages within Chrysomyxa pyrolae and Chrysomyxa rhododendri, providing some evidence for allopatric speciation within these morphologically defined species. This finding, together with the observed pattern of host specificities of the studied rust fungi suggest that species diversification within the C. ledi species complex might be governed by a set of factors, such as specialisation to certain Ericaceae species as telial hosts and, to a lesser extent, specialisation to different spruce species as aecial hosts. Moreover, allopatric speciation by geographic disruption of species also seems to take place. Unexpectedly, when our data were integrated into a broader phylogenetic framework, the Chrysomyxa genus was not resolved as a monophyletic group. Indeed, the spruce cone rusts C. pyrolae and C. monesis coalesced with the pine needle rusts belonging to the genus Coleosporium, whereas the microcyclic species Chrysomyxa weirii was embedded within a clade comprising the genus Melampsora.