The genomic architecture and molecular mechanisms controlling variation in quantitative disease resistance loci are not well understood in plant species and have been barely studied in long-generation trees. Quantitative trait loci mapping and genome-wide association studies were combined to test a large single nucleotide polymorphism (SNP) set for association with quantitative and qualitative white pine blister rust resistance in sugar pine. In the absence of a chromosome-scale reference genome, a high-density consensus linkage map was generated to obtain locations for associated SNPs. Newly discovered associations for white pine blister rust quantitative disease resistance included 453 SNPs involved in wide biological functions, including genes associated with disease resistance and others involved in morphological and developmental processes. In addition, NBS-LRR pathogen recognition genes were found to be involved in quantitative disease resistance, suggesting these newly reported genes are qualitative genes with partial resistance, they are the result of defeated qualitative resistance due to avirulent races, or they have epistatic effects on qualitative disease resistance genes. This study is a step forward in our understanding of the complex genomic architecture of quantitative disease resistance in long-generation trees, and constitutes the first step towards marker-assisted disease resistance breeding in white pine species.