The South China Mainland (SCM) and its adjacent continental islands are a global biodiversity hotspot. However, how and when plants dispersed between SCM and Hainan/Taiwan Islands remains largely unknown. In this study, we used restriction site-associated DNA sequencing (RAD-seq) to identify the demographic dynamics and local adaptation of Quercus championii, a dominant forests tree distributed in SCM and Hainan/Taiwan Islands. Through phylogenetic reconstruction, principal components analysis (PCA) and structure analysis, we identified four distinct Q. championii lineages that correspond to its geographical distribution. The genetic structure of Hainan Island population was distinct, possibly reflecting an introgression. We conducted an approximate Bayesian computation analyses and found that Q. championii originated from Southwest China-Northern Vietnam, then dispersed to Southeast China as the climate warmed. During the Pleistocene glacial period, land bridges arose between SCM and Hainan/Taiwan Islands, and the land bridges likely facilitated species dispersal from SCM to these islands. We found a strong correlation between genetic variation and isothermality through a gradient forest analysis and identified precipitation seasonality as a key driver to the local adaptation of Q. championii. Finally, we analyzed putative adaptation loci and identified genes regulating vegetative and reproductive organ development as important for the adaptation of Q. championii to heterogeneous environments. We provide new insights into the evolutionary history and local adaptation of biotas in Southern China and adjacent islands.