Capsule-negative Haemophilus influenzae, also known as non-typeable H. influenzae (NTHi), is an opportunistic Gram-negative pathogen that exclusively infects humans. Although a common commensal in the upper respiratory tract, NTHi is associated with many acute and chronic diseases including otitis media, bronchiectasis and COPD. NTHi genomes have variable gene content and there is evidence for frequent gene exchange with related species. Further, NTHi and other Haemophilus species are commonly co-isolated from the respiratory tract and can be phenotypically indistinguishable. Accurate identification of NTHi has therefore proven to be a non-trivial endeavour. Here, we used whole-genome sequencing to characterise 97 Australian Haemophilus isolates, including 68 NTHi, from Northern Territory, Western Australia and Queensland. Isolates were from nasopharyngeal carriage, bronchiectasis (bronchoalveolar lavage) and neonatal bacteraemia. The outcomes from our study were fourfold. First, phylogenetic analysis based on core orthologous single-nucleotide polymorphisms showed, for the first time, a clear delineation between H. influenzae (including NTHi) and closely related species, such as the non-pathogenic Haemophilus haemolyticus. Second, we demonstrate that 1.0Mb (52%) of the H. influenzae genome is shared amongst strains globally, but only 24kb (1.2%) is unique and common to H. influenzae. We used these data to design a H. influenzae-specific real-time PCR assay targeting the fucP locus, which overcomes issues of false-positives and -negatives with existing assays. Third, comparison of disease (i.e. lower respiratory tract and blood) and asymptomatic carriage (i.e. upper respiratory tract) associated isolates showed no significant gene content differences or phylogenetic clustering, indicating that carriage is a prerequisite for disease. Last, we demonstrate that Australian NTHi are not distinct from NTHi from other continents, suggesting person-to-person transmission on a global scale. Our study answers fundamental questions about the Haemophilus genus and highlights research areas that remain to be addressed.