In the post-Haemophilus influenzae type b (Hib) vaccine era, invasive H. influenzae type a (Hia) disease emerged in North American Indigenous populations. The role of Hia in non-invasive disease is uncertain; it is unknown if non-invasive Hia infections are prevalent in populations with high incidence of invasive disease, and whether invasive and non-invasive Hia isolates have different characteristics. We analyzed all invasive and non-invasive clinical H. influenzae isolates collected in a Northwestern Ontario hospital serving 82% Indigenous population over 5.5 years. Serotyping, clonal analysis, and antimicrobial sensitivity testing was conducted on 233 non-invasive and 20 invasive isolates. Among non-invasive isolates, 91% were non-typeable (NTHi), 3% were Hia; Hia was the most frequent invasive isolate (60%). Incidence rates of invasive H. influenzae disease (12.5/100,000/year) greatly exceeded average provincial data, with highest found in <6-year-old children (63.9/100,000/year); proportion of Hia among invasive isolates was 7 times larger than in Ontario. No difference in clonal characteristics between invasive and non-invasive Hia isolates was found. Antibiotic resistance was more common among NTHi than among encapsulated isolates, without differences between invasive and non-invasive isolates. Considering significance of Hia in Indigenous populations, pediatric immunization against Hia will be useful to prevent serious infections in young Indigenous children.