Huanglongbing (HLB), caused by ‘Candidatus Liberibacter asiaticus’ (CLas), poses a major threat to citrus production worldwide and has recently emerged as a serious constraint to sweet orange cultivation in Bangladesh. Despite widespread disease occurrence, information on the genetic diversity of CLas populations in the country is lacking. This study investigated the genetic structure of CLas across major sweet orange–growing regions of Bangladesh using tandem repeat number (TRN) variation at the CLIBASIA_01645 genomic locus. Field surveys were conducted in 17 districts between 2022 and 2023, and 89 HLB-symptomatic leaf samples were collected from commercial orchards. PCR and qPCR detection confirmed CLas infection in 67 (75%) and 74 (83%) samples, respectively. Thirty-seven representative isolates were sequenced and analyzed for TRN polymorphism. Ten TRN genotypes (TRN2–TRN12, excluding TRN3) were identified, with TRN6 being the most prevalent. Bangladeshi CLas isolates were further grouped into three classes based on TRN: Class I (TRN ≤ 5), Class II (5 < TRN ≤ 10), and Class III (10 < TRN ≤ 15), of which Class II was the predominant. All Bangladeshi isolates harbored the CTTGTGT repeat motif and clustered closely with Indian isolates in haplotype network and phylogenetic analyses, while isolates carrying the AGACACA motif from other countries formed a distinct clade. These results reveal intraspecific diversity of CLas in Bangladesh and suggest regional structuring and shared ancestry with neighboring Indian populations. This study provides the first population-level genetic insight into CLas in Bangladesh and establishes a foundation for improved epidemiological understanding and disease management.