The first genetic linkage map was made over 100 years ago and for the past few decades maps made from molecular markers have been fundamental tools for marker-assisted breeding, quantitative trait loci identification and gene identification by map-based cloning. The advent of next-generation sequencing technologies has revolutionised genetic marker identification, enabling construction of high-density genetic maps containing tens of thousands to millions of sequence-characterised markers. These maps can be used for new purposes, such as anchoring genome assemblies and genome-wide analysis of recombination rate. We have developed a high-density genetic map for the flax rust fungus, Melampsora lini, a plant pathogen and model for understanding the biology of agriculturally important rust fungi. The map comprises 13,412 restriction site-associated DNA sequencing (RADseq) markers in 27 linkage groups that together span 5,860 cM and contain 2,756 recombination bins. The marker sequences were used to anchor 68.9% of the M. lini genome assembly onto the genetic map. The map and anchored assembly were then used to: 1) show that M. lini has a high overall meiotic recombination rate, but recombination distribution is uneven and large coldspots exist; 2) show that substantial genome rearrangements have occurred in spontaneous loss-of-avirulence mutants; and 3) identify the AvrL2 and AvrM14 avirulence genes by map-based cloning.