Rust fungi (order Pucciniales) form the largest group of pathogens that threaten plants of economic and ecological significance. Rust fungi have multiple spore stages and are dikaryotic during asexual propagation, with each nucleus containing a full set of haploid chromosomes. Traits like virulence therefore obey diploid genetic inheritance. Additionally, rust fungi can exchange whole nuclei. Advances in genomics are now delivering nuclear-phased genomes which can be harnessed to determine migration, population structure but also to characterize variation at effector loci to better understand how virulence evolution occurs. We describe a pan-genome for the causal agent of wheat stem rust Puccinia graminis f. sp. tritici (Pgt), including the races TTKSK (Ug99), TKTTF (ETH2013-1) and TTRTF (ITA2018-1) all of which caused significant epidemics in East Africa or Europe. We compiled a catalogue of genetic variants for seven Avr genes in four major lineages of Pgt and tested these for recognition by the corresponding wheat resistance genes, which delivers a molecular explanation for the virulence phenotypes of lineages. Lastly, we show how combining a high-throughput protoplast screening platform with improved effector gene annotations is enabling the rapid identification of additional, novel rust effectors from nuclear-phased genomes. This Pgt Avr effector gene atlas represents a significant milestone towards predicting virulence and epidemiology and will enable a monitoring system where we anticipate rather than respond to pathogen evolution.