Chikungunya virus (CHIKV) causes recurrent epidemics across tropical and subtropical regions globally. In 2025, Guangdong reported mainland China's largest documented CHIKV outbreak, with 23,464 cases across all 21 prefecture-level cities. Integrating epidemiological, genomic, and phylodynamic analyses, we investigated the outbreak's origins, transmission, and viral adaptation. The Guangdong strain belonged to the ECSA-MAL lineage, exhibiting a long internal branch that highlights significant global surveillance gaps. Phylodynamic modeling estimated viral introduction in early April 2025, revealing ~2.5 months of cryptic transmission alongside rising vector densities. Spatial case distribution was moderately associated with human mobility from the epicenters. Globally, phylogenetic analysis identified 33 potential adaptive mutations across nine proteins and 14 epidemic lineages, including validated and 15 novel mutations. Twelve novel mutations occurred in the Asian Urban lineage (AUL), predominantly affecting NSP3. This study underscores the need for enhanced pre-peak surveillance and continuous monitoring of viral adaptation across ecological regions.