Cultivated chrysanthemum (Chrysanthemum morifolium Ramat.) is an economically important ornamental plant species grown worldwide. However, the origin of the genus Chrysanthemum remains unclear. This study was conducted in the Hengduan Mountains, Yunnan Province. We took advantage of a special geographic region where the southernmost species of Ajania and the highest altitude population of Chrysanthemum indicum coexist to investigate their evolutionary origins. Diversity analysis of 9 populations of 5 species that came from 3 genera was carried out based on morphological traits and SRAP markers. Furthermore, topographical and ecological analyses and surveys of the vegetation communities in the plots were carried out for correlation analysis, and past data were used to reconstruct the ancient topography and vegetation to estimate the migration path and divergence time. We found that Chrysanthemum and Ajania were closely related based on the smooth transition states among marginal female florets and their common pollination system. The genetic relationship between Phaeostigma and Chrysanthemum was relatively distant, and Ajania was between them. Low light intensity and relatively humid habitats may be driving the elongation and evolution of marginal female florets. We found that Chrysanthemum and related genera were largely restricted to stony topographies at an altitude of ~3000 m.a.s.l. and in specialized alpine coniferous (Pinus) and broad-leaved (Quercus) mixed forest marginal communities. These stony topographies have become ecological islands of refuge for these species in the current interglacial period. The Hengduan Mountains play a key role in the evolution, divergence, and survival of Chrysanthemum and its allies.