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Summary White oak (Quercus alba) is an abundant forest tree species across eastern North America that is ecologically, culturally, and economically important.We report the first haplotype‐resolved chromosome‐scale genome assembly ofQ. albaand conduct comparative analyses of genome structure and gene content against other published Fagaceae genomes. We investigate the genetic diversity of this widespread species and the phylogenetic relationships among oaks using whole genome data.Despite strongly conserved chromosome synteny and genome size acrossQuercus, certain gene families have undergone rapid changes in size, including defense genes. Unbiased annotation of resistance (R) genes across oaks revealed that the overall number of R genes is similar across species – as are the chromosomal locations of R gene clusters – but, gene number within clusters is more labile. We found thatQ. albahas high genetic diversity, much of which predates its divergence from other oaks and likely impacts divergence time estimations. Our phylogenetic results highlight widespread phylogenetic discordance across the genus.The white oak genome represents a major new resource for studying genome diversity and evolution inQuercus. Additionally, we show that unbiased gene annotation is key to accurately assessing R gene evolution inQuercus.