Bacterial blight (BB), caused by Xanthomonas oryzae pv. oryzae (Xoo), is a serious constraint to basmati rice production. The increasingly evident outbreaks of BB in recent years necessitate an immediate search for ecology-conscious, cost-effective and durable management strategy. Given the context, this investigation aimed to generate knowledge about the haplotypic and pathogenic variability of Xoo population severely affecting Pusa Rice Hybrid 10 (PRH-10), world’s first superfine aromatic basmati hybrid. Seven haplotypes were detected from the experimental field applying two PCR-based assays, i.e. repetitive sequence-based polymerase chain reaction and insertion sequence based PCR. The experimental results revealed greater genetic heterogeneity in the Xoo population with high value of total haplotypic diversity (HT = 0.79). In addition, based on the virulence assay, the genetic heterogeneity corresponded to the presence of four pathotypes. Importantly, the substantial line × strain interactions was significant (p ≤ 0.01), which confirmed the host specificity in the system. In parallel, it was noted that most of the key resistance genes except Xa21, deployed in the rice breeding program at International Rice Research Institute were overcome by the Xoo strains, thus underscoring the relevance of this gene in resistance breeding. Therefore, incorporating Xa21 alone, or in combination with xa13 or xa5 into the parental lines, using various modern genomics-assisted approaches might be the potential fast-track strategy to breed PRH-10 with remarkably enhanced BB resistance. The present investigation provides a molecular framework for future epidemiological studies and is likely to assist rice breeders to expedite basmati rice improvement.