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The lungs, once considered sterile, are now known to contain diverse, dynamic microbial communities that are metabolically active and immunologically consequential even in health. In respiratory disease, these communities undergo quantitative and compositional changes that predict clinical trajectories and may contribute to pathogenesis. The past decade of research has advanced our understanding of the complex bidirectional relationship between the respiratory tract and the microbial communities it encounters. In health, the lungs are nutrient poor and defended by robust host defences, limiting local microbial growth and keeping bacterial populations sparse and transient. Yet, in respiratory disease, the ecological conditions of the lungs permit and promote the outgrowth of select microorganisms. Recent in vivo and ex vivo discoveries explain how this respiratory dysbiosis is both a cause and a consequence of airway and alveolar injury. To leverage the respiratory microbiome for therapeutic benefit, we must interrogate both how disease-altered microbial communities shape immune responses, treatment efficacy and outcomes, and how host and environmental factors, in turn, shape the respiratory microbiome. In this Review, we synthesize current insights into how the respiratory microbiome contributes to chronic and acute lung diseases and explore its clinical implications for diagnosis, prognosis and therapy.