Moraxella catarrhalis is an important cause of infectious exacerbations of chronic obstructive pulmonary disease and otitis media. To investigate the population structure of M. catarrhalis, we developed a core-genome multilocus sequence typing (cgMLST) scheme using 1319 core genes, and a life identification number (LIN) barcode classification system. Whole-genome analyses of nearly 2000 genomes confirmed divergent seroresistant (SR) and serosensitive (SS) M. catarrhalis lineages with distinct evolutionary trajectories. SR genomes are more conserved, while SS genomes exhibited greater genetic variability. Virulence gene analyses revealed lineage-specific variations in ubiquitous surface proteins (UspA1 and UspA2) and lipooligosaccharide (LOS) types. The bro β-lactamase, and mcb bacteriocin cluster, are more common in SR lineages, which suggested different selective pressures and adaptation. Here, we show that this cgMLST scheme and LIN code system provide a robust method for characterising M. catarrhalis, distinguish between SR and SS lineages, and offer a unified framework for population structure analyses.