Infectious exacerbations of chronic lung diseases like cystic fibrosis (CF) and chronic obstructive pulmonary disease (COPD) are a major cause of morbidity and mortality worldwide. These exacerbations are frequently caused by opportunistic infectious microbes – predominantly bacteria – and are associated with a more rapid disease progression, diminished quality of life, greater healthcare burden and increased mortality. Increasingly affordable microbial metagenomic (MMG) and metatranscriptomic (MMT) approaches, which capture enriched microbial DNA and RNA from clinical specimens to the exclusion of host nucleic acids, offer exciting opportunities for the personalised diagnosis, monitoring and informed treatment of chronic lung infections. Here, we used MMT and MMG to examine the microbial basis of exacerbations in CF and COPD airways, respectively. When compared with standard 16S rRNA profiling, MMT revealed much greater insights into microbial activity within CF airways, with a dominance of P. aeruginosa and evidence of antimicrobial resistance determinants, indicating ineffectiveness of antimicrobial therapy for pathogen eradication. In COPD, MMG unveiled a diverse microbial landscape largely missed using standard clinical laboratory culturing methods. Few or no participants had ‘common’ COPD pathogens (Haemophilus influenzae, Streptococcus pneumoniae, Moraxella catarrhalis). Instead, COPD exacerbations were dominated by opportunistic bacteria, including Pantoea, Cellulosimicrobium, Pseudmonas fluorescens group, and Rothia mucilaginosa, which may contribute to a higher burden of COPD exacerbations than currently appreciated. Finally, our MMG results, whilst preliminary, identified two bacteria – Comamonas and Raoultella – significantly associated with people with COPD who had lung cancer as a comorbidity. Taken together, our study demonstrates the feasibility and exciting opportunities afforded by meta-omics approaches for comprehensively cataloguing the microbes associated with chronic lung diseases.