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Abstract The development of strawberry (Fragaria × ananassa Duchesne ex Rozier) cultivars resistant to Phytophthora crown rot (PhCR), a devastating disease caused by the soil‐borne pathogen Phytophthora cactorum (Lebert & Cohn) J. Schröt., has been challenging partly because the resistance phenotypes are quantitative and only moderately heritable. To develop deeper insights into the genetics of resistance and build the foundation for applying genomic selection, a genetically diverse training population was screened for resistance to California isolates of the pathogen. Here we show that genetic gains in breeding for resistance to PhCR have been negligible (3% of the cultivars tested were highly resistant and none surpassed early 20th century cultivars). Narrow‐sense genomic heritability for PhCR resistance ranged from 0.41 to 0.75 among training population individuals. Using multivariate genome‐wide association studies (GWAS), we identified a large‐effect locus (predicted to be RPc2) that explained 43.6–51.6% of the genetic variance, was necessary but not sufficient for resistance, and was associated with calcium channel and other candidate genes with known plant defense functions. The addition of underutilized gene bank resources to our training population doubled additive genetic variance, increased the accuracy of genomic selection, and enabled the discovery of individuals carrying favorable alleles that are either rare or not present in modern cultivars. The incorporation of an RPc2‐associated single‐nucleotide polymorphism (SNP) as a fixed effect increased genomic prediction accuracy from 0.40 to 0.55. Finally, we show that parent selection using genomic‐estimated breeding values, genetic variances, and cross usefulness holds promise for enhancing resistance to PhCR in strawberry.