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Leaf scald caused by <i>Xanthomonas albilineans</i> (<i>Xa</i>) is a major bacterial disease in sugarcane that represents a threat to the global sugar industry. Little is known about the population structure and genetic evolution of this pathogen. In this study, 39 <i>Xa</i> strains were collected from 6 provinces in China. Of these strains, 15 and 24 were isolated from <i>Saccharum</i> spp. hybrid and <i>S. officinarum</i> plants, respectively. Based on multilocus sequence analysis (MLSA), with five housekeeping genes, these strains were clustered into two distinct phylogenetic groups (I and II). Group I included 26 strains from 2 host plants, <i>Saccharum</i> spp. hybrid and <i>S. officinarum</i> collected from 6 provinces, while Group II consisted of 13 strains from <i>S. officinarum</i> plants in the Zhejiang province. Among the 39 <i>Xa</i> strains, nucleotide sequence identities from 5 housekeeping genes were: <i>ABC</i> (99.6–100%), <i>gyr</i>B (99.3–100%), <i>rpo</i>D (98.4–100%), <i>atp</i>D (97.0–100%), and <i>gln</i>A (97.6–100%). These strains were clustered into six groups (A–F), based on the rep-PCR fingerprinting, using primers for ERIC2, BOX A1R, and (GTG)5. UPGMA and PCoA analyses revealed that group A had the most strains (24), followed by group C with 11 strains, while there was 1 strain each in groups B and D–F. Neutral tests showed that the <i>Xa</i> population in <i>S. officinarum</i> had a trend toward population expansion. Selection pressure analysis showed purification selection on five concatenated housekeeping genes from all tested strains. Significant genetic differentiation and infrequent gene flow were found between two <i>Xa</i> populations hosted in <i>Saccharum</i> spp. hybrids and <i>S. officinarum</i>. Altogether, these results provide evidence of obvious genetic divergence and population structures among <i>Xa</i> strains from China.