Huanglongbing (HLB; greening disease), caused by Candidatus Liberibacter asiaticus (CLas), is the most damaging citrus disease worldwide. The disease has spread throughout the citrus-producing regions of Guangxi, Guangdong, Fujian, and others in China. A total of 1,789 HLB-like symptomatic or asymptomatic samples were collected from the Guangxi and Fujian provinces of China to decipher the genetic diversity of CLas and its correlation with pathogenicity and host range. The disease was the most severe in orange and the least in pomelo. CLas bacteria associated with the specific geographical and citrus variety infected more than 50% of the HLB-like symptomatic samples. We identified a total of 6,286 minor variations by comparing 35 published CLas genomes and observed a highly heterogeneous variation distribution across the genome. Highly diverse regions, including two prophages, were generally more unstable and prone to lose. In the collected CLas strains, four highly diverse non-prophage segments and three prophage segments in the prophage region were chosen for PCR amplification and genotyping. Four hypervariable regions were used to decipher CLas diversity. A total of 100 strains were divided into four groups, of which 90 strains were clustered into two clades with 15 reported reference genomes, while 10 were grouped in two clades separately from the reported genomes. This study provides insight into the molecular characteristics and genetic variations of different CLas strains in China and might help develop HLB prevention and control strategies.