A Microviridae phage CLasMV1, was recently identified in “Candidatus Liberibacter asiaticus” (CLas), the bacterium associated with citrus Huanglongbing (HLB). The CLasMV1 strain GDHZ11D (CP045566) exhibited a circular genome of 8,869 bp containing eight open reading frames (ORFs). Phages of CLas play crucial roles in regulating bacterial population diversity that have potential use for HLB control. However, knowledge of CLasMV1 population diversity is currently limited. In this study, 1,520 CLas samples were collected from 10 citrus-growing provinces in China. PCR screening revealed that 1,042 samples (69%) harbored CLasMV1. Complete genome sequences of 43 CLasMV1 strains were obtained through Illumina HiSeq sequencing with genome size ranging from 8,696 bp to 8,881 bp. Variations were mostly related to single-nucleotide polymorphisms (SNPs) and sequence insertion/deletions (In/Dels). Notably, two hypervariable regions (HVRs) were identified. Two new ORFs were detected, ORFA (144 bp) in HRV-1 and ORFB (342 bp) in HRV-2. Whole genome phylogenetic analysis using 43 strains from this study, nine previously reported Chinese strains, and two Florida strains (CP040636, MZ382797) delineated five genomic groups. Chinese strains dominated Groups 1 to 4, while Group 5 contained the Florida strains. Further analyses of the HVR-1 across all 1,042 CLasMV1 samples detected a 173-bp sequence with suspected mobile activity. Analysis of PacBio long read assembly published previously detected a concatemer of CLasMV1 sequence, suggesting that the phage used the rolling-cycle mechanism for its replication. These findings significantly enhance our understanding of CLasMV1 genomic diversity and will facilitate future research in CLasMV1 classification and HLB biology.