The recent emergence of highly pathogenic avian influenza (HPAI) in dairy cattle has raised concerns about potential non-respiratory exposure routes including ingestion of contaminated raw milk. In this study, we assessed the survival of influenza A virus (IAV) in milk during simulated human digestion and estimated infection risk using quantitative microbial risk assessment (QMRA). Whole milk artificially inoculated with IAV A(H1N1) was exposed to human saliva, fed-state simulated gastric fluids (pH 3–6) containing pepsin, and fed-state simulated intestinal fluids containing pancreatin, in the presence or absence of mucin. Viral infectivity was quantified using plaque assays. Exposure to saliva did not reduce viral infectivity, whereas gastric inactivation was strongly pH-dependent, ranging from approximately 1 log reduction at pH 6 to about 6 log reduction at pH 3. Complete viral inactivation (>6 log10) was observed following exposure to fed-state intestinal fluid, regardless of mucin presence. Mucin conferred partial protection against gastric inactivation at pH 3 and 4.5. QMRA incorporating experimentally derived inactivation data estimated median probabilities of infection per serving ranging from 1.35 × 10-5 to 1.35 × 10-8 under four dose–response assumptions. Overall, these results indicate that human digestion substantially reduces the infectivity of influenza viruses in contaminated milk and provide quantitative evidence to inform food safety risk assessments for influenza viruses and other enveloped viruses potentially transmitted through raw dairy products.