Streptococcus pneumoniae coinfection is a major cause of influenza‐associated mortality; however, the mechanisms underlying pathogenesis or protection remain unclear. Using a clinically relevant mouse model, we identify immune‐mediated damage early during coinfection as a new mechanism causing susceptibility. Coinfected CCR2^−/− mice lacking monocytes and monocyte‐derived cells control bacterial invasion better, show reduced epithelial damage and are overall more resistant than wild‐type controls. In influenza‐infected wild‐type lungs, monocytes and monocyte‐derived cells are the major cell populations expressing the apoptosis‐inducing ligand TRAIL. Accordingly, anti‐TRAIL treatment reduces bacterial load and protects against coinfection if administered during viral infection, but not following bacterial exposure. Post‐influenza bacterial outgrowth induces a strong proinflammatory cytokine response and massive inflammatory cell infiltrate. Depletion of neutrophils or blockade of TNF‐α facilitate bacterial outgrowth, leading to increased mortality, demonstrating that these factors aid bacterial control. We conclude that inflammatory monocytes recruited early, during the viral phase of coinfection, induce TRAIL‐mediated lung damage, which facilitates bacterial invasion, while TNF‐α and neutrophil responses help control subsequent bacterial outgrowth. We thus identify novel determinants of protection versus pathology in influenza–Streptococcus pneumoniae coinfection.