SUMMARY Camellia plants include more than 200 species of great diversity and immense economic, ornamental, and cultural values. We sequenced the transcriptomes of 116 Camellia plants from almost all sections of the genus Camellia. We constructed a pan‐transcriptome of Camellia plants with 89 394 gene families and then resolved the phylogeny of genus Camellia based on 405 high‐quality low‐copy core genes. Most of the inferred relationships are well supported by multiple nuclear gene trees and morphological traits. We provide strong evidence that Camellia plants shared a recent whole genome duplication event, followed by large expansions of transcription factor families associated with stress resistance and secondary metabolism. Secondary metabolites, particularly those associated with tea quality such as catechins and caffeine, were preferentially heavily accumulated in the Camellia plants from section Thea. We thoroughly examined the expression patterns of hundreds of genes associated with tea quality, and found that some of them exhibited significantly high expression and correlations with secondary metabolite accumulations in Thea species. We also released a web‐accessible database for efficient retrieval of Camellia transcriptomes. The reported transcriptome sequences and obtained novel findings will facilitate the efficient conservation and utilization of Camellia germplasm towards a breeding program for cultivated tea, camellia, and oil‐tea plants. Significance Statement High‐quality transcriptomes of 116 Camellia plants from almost all sections of genus Camellia unveils their deep phylogeny and the transcriptional mechanism underlying the dynamic evolution of quality traits related secondary metabolites, which will facilitate the efficient conservation and utilization of Camellia germplasm towards a breeding program for cultivated tea, camellia, and oil‐tea plants.