Camellia contains tea, oil camellia, and camellias which benefit people globally. Its infrageneric classification is, however, controversial and unstable, and former phylogenetic analyses failed to yield robust and consistent trees. Here, we aimed to reconstruct a robust phylogenetic tree, date all clades and discuss the evolutionary history of Camellia. Emphasizing the taxonomically comprehensive sampling rather than more DNA data, orthologous nuclear RPB2 introns 11-15 and 23, and waxy were sequenced for 99 taxa of Camellia to reconstruct its phylogenetic history. Ten clades are identified in Camellia: Camellia II, Camelliopsis, Corallina, Furfuracea, Heterogenea, Paracamellia, Piquetia, Stereocarpus, Thea and Yellow camellias II. Camellia grijsii and C. shensiensis are not closely related with other oil camellias that form the clade Paracamellia. Sections Camelliopsis and Theopsis together form the clade Camelliopsis, while clade Furfuracea consists of sect. Furfuracea and C. hongkongensis. Camellia connata is separated from C. lanceolata but nested in the clade Heterogenea, and C. longissima is nested in the clade Thea, suggesting a new germplasm for tea breeding. Molecular dating using four fossil calibration points suggests that the crown age of Camellia is 39.5 Ma with clade Corallina probably the earliest infrageneric clade to diversify and the most widespread clade, Paracamellia, the latest. Our findings provide new insights into the phylogenetic relationships, systematics and evolutionary history of Camellia.