<p>Oil camellias are important edible oil sources that are widely cultivated in South China and Indochina. <i>Camellia osmantha</i> C.X. Ye, J.L. Ma &amp; H. Ye, an oil camellia that was described in 2012, has generated several high-yield cultivars in Guangxi, China. However, its genetic diversity and structure have not been adequately explored. Based on nuclear genomic single-nucleotide polymorphisms harvested from double digest restriction-site-associated DNA sequencing,Query 35 samples of <i>C. osmantha</i> and 26 individuals of other oil camellias in <i>C.</i> sect. <i>Paracamellia</i> were analyzed to reveal their population genetic and phylogenetic characteristics. Populations of <i>C. osmantha</i> bore a generally higher expected heterozygosity (<i>H</i>_E = 0.1029–0.1750) and nucleotide diversity (<i>π</i> = 0.1537–0.1976) compared with other camellias, which may suggest a relatively high level of genetic diversity has been conserved during artificial selection. Ancestry analysis revealed a roughly homogeneous and identical genetic background of all individuals of <i>C. osmantha</i>, which was distinct from other camellias and verified in principal component analysis. Phylogenetic investigation supported the specific status of <i>C. osmantha</i> and revealed four main clades within the species. The selected and named cultivars of <i>C. osmantha</i> can be found in each clade, implying a relatively representative genetic selection during its breeding.</p>