Haemophilus influenzae biogroup aegyptius (H. aegyptius) is a bacterial species which typically causes purulent conjunctivitis in children, but is also the causative agent of a severe invasive disease with high mortality, Brazilian Purpuric Fever (BPF), similar in symptomatic presentation to meningitis. Cases of BPF have emerged sporadically for over 40 years. Though strains of H. aegyptius which cause BPF are distinct from non-BPF strains, it is not known what factors contribute to the manifestation of BPF. Phase variation is the rapid and reversible switching of gene expression. Many bacterial pathogens encode phase-variable methyltransferases as part of restriction modification (R-M) systems. These systems are known as phasevarions (phase-variable regulons), and result in variable expression of multiple genes through phase variation of a single enzyme. Phasevarions have been shown to be key regulators of pathobiology in many host-adapted pathogens. The majority of the phasevarions characterised to date result from the ON-OFF switching of Type III DNA methyltransferases (Mod), encoded by mod genes. H. aegyptius encodes the Type III methyltransferase ModA16. ModA methyltransferases in related Haemophilus species, such as non-typeable Haemophilus influenzae (NTHi) have been demonstrated to be phase-variable, and control phasevarions. In this study, we demonstrate that expression of ModA16 is subject to biphasic ON-OFF switching due to variation in length of a locus encoded simple sequence repeat tract. Single-Molecule, Real-Time (SMRT) sequencing showed that ModA16 methylates the sequence GGRC(m6)A, and that differential methylation of this sequence results in altered expression of multiple proteins, determined by quantitative proteomics (SWATH-ms). Proteins with altered expression include several virulence factors, and numerous outer membrane proteins including those which have been implicated in the development of BPF. Characterisation of this previously undescribed phasevarion may provide knowledge on the sporadic emergence of BPF-causing strains of H. aegyptius and direct future treatment strategies.