Clematis, known as the Queen of climbers, is a genus in Ranunculaceae with a great number of climbing species. It is of great horticultural values and has earned popularity among gardeners. Although several molecular phylogenetic studies based on a few DNA segments have been conducted, the relationships among major groups of Clematis remain controversial, and the evolution of the self-supported or shrubby species is still unknown. In this study, we assembled the complete plastome and nrDNA sequences of 56 Clematis species representing most of the sections of the genus and reconstructed phylogenetic framework of the genus using both datasets. Our sampling also covered all species of C. sect. Fruticella s. s. and related taxonomically controversial species to test the monophyly of the section and evolution of different habits of Clematis. The complete plastome and nrDNA sequences obtained similar phylogenetic frameworks of Clematis using both likelihood and Bayesian methods, but they also contradicted in many ways. The complete plastome sequence analysis obtained a better resolved phylogeny than nrDNA sequence. From the complete plastome phylogeny, we obtained five well resolved major clades for all the sampled species, except a first diverged African species. The results also indicated that many of the morphological characters that had been widely used for taxonomy were results of parallel and convergent evolution. Molecular dating results demonstrated that all the major clades of Clematis have radiated during the onset of Pliocene. The genus has also experienced species radiation during the Quaternary. The erect and shrubby habits of Clematis may have evolved multiple times. Clematis sect. Meclatis was revealed to be sister to C. sect. Fruticella. Species of C. sect. Fruticella diversified during late Quaternary. We hypothesized that the cold and dry climate during Quaternary may have facilitated species diversification and dispersal of C. sect. Fruticella.