A population of 239 perennial ryegrass (Lolium perenne L.) genotypes was analyzed to identify marker-trait associations for crown rust (Puccinia coronata f. sp. lolii) and brown rust (Puccinia graminis f. sp. loliina) resistance. Phenotypic data from field trials showed a low correlation (r = 0.17) between the two traits. Genotypes were resequenced, and a total of 14,538,978 SNPs were used to analyze population structure, linkage disequilibrium (LD), and for genome-wide association study. The SNP heritability (h2SNP) was 0.4 and 0.8 for crown and brown rust resistance, respectively. The high-density SNP dataset allowed us to estimate LD decay with the highest possible precision to date for perennial ryegrass. Results showed a low LD extension with a rapid decay of r2 value below 0.2 after 520 bp on average. Additionally, QTL regions for both traits were detected, as well as candidate genes by applying Genome Complex Trait Analysis and Multi-marker Analysis of GenoMic Annotation. Moreover, two significant genes, LpPc6 and LpPl6, were identified for crown and brown rust resistance, respectively, when SNPs were aggregated to the gene level. The two candidate genes encode proteins with phosphatase activity, which putatively can be induced by the host to perceive, amplify and transfer signals to downstream components, thus activating a plant defense response.