Studies have indicated the potential importance of the human nasal and respiratory microbiomes in health and disease. However, the roles of these microbiomes in the pathogenesis of influenza and its complications are not fully understood. Therefore, the objective of this systematic review and analysis is to identify the patterns of nasal and respiratory microbiome dysbiosis and to define the unique signature bacteria associated with influenza compared with other respiratory tract infections. We compared the respiratory microbiome composition between influenza patients and healthy controls; across different influenza severities; in adult versus pediatric influenza patients; as well as influenza versus other respiratory infections. The desired outcomes include the signature bacteria in each cohort and the Shannon index to reflect the alpha diversity. Of the 2269 articles identified, 31 studies fulfilled the inclusion criteria. These studies investigated the respiratory tract microbiomes of patients with influenza, COVID-19, pneumonia, other respiratory infections, and chronic rhinosinusitis (CRS). Our review revealed that the phylum Firmicutes and Actinobacteria, genus Actinomyces, Streptococcus and Granulicatella, and species Neisseria are more prominent in severe influenza than mild to moderate influenza. Reduced microbiome alpha diversity is noted in influenza patients compared to healthy controls. There are some similarities and differences between the signature bacteria in pediatric and adult influenza patients, e.g., Streptococcus is common in both age groups, whereas Pseudomonas is associated with adults. Intriguingly, there is a common predominance of Streptococcus and Firmicutes among influenza and pneumonia patients. COVID-19 patients exhibit an increased abundance of Firmicutes as well as Pseudomonas. In CRS patients, Proteobacteria and Haemophilus are found in high abundance. This review highlights some similarities and differences in the respiratory microbiomes and their signature organisms in influenza of varying severity and in different age groups compared with other respiratory infections. The dysbiosis of the respiratory microbiomes in these respiratory infections enhances our understanding of their underlying pathogenic mechanisms.