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The global demand for sustainable protein sources is rapidly increasing due to environmental pressures associated with conventional livestock production. This study integrates regional waste statistics, spatial analysis, and species-specific bioconversion modelling to estimate the theoretical potential of compostable municipal waste for insect-derived protein production in Slovakia. Regional data on municipal waste generation and treatment were obtained from the Statistical Office of the Slovak Republic for eight NUTS-3 administrative regions (2024 baseline). Two complementary approaches were applied: a conservative empirical approach based on R03 organic recovery flows, and a model-based estimation using 40% of total municipal waste as the organic fraction (OFMSW). Four insect species were evaluated: Hermetia illucens (black soldier fly), Tenebrio molitor (yellow mealworm), Acheta domesticus (house cricket), and Locusta migratoria (migratory locust). Biomass conversion was modelled using deterministic mass-balance equations with species-specific bioconversion efficiencies (0.16–0.20 kg DM per kg substrate DM) and protein content coefficients (47–60% DM), each selected as the mid-range estimate from primary experimental literature. The results reveal pronounced regional heterogeneity in compostable substrate availability, with western and densely populated regions exhibiting the highest absolute quantities. Protein production potential varied substantially across species and regions, with T. molitor demonstrating both the highest biomass yield and the highest protein production density per unit substrate, while L. migratoria exhibited the highest protein content per unit produced biomass. Expanded sensitivity analysis (±30% for bioconversion yield coefficients, ±15% for dry matter fraction, ±10% for protein content) confirmed the directional robustness of model outputs while quantifying the substantial uncertainty range inherent in regional bioconversion estimates. A regulatory scenario based on Regulation (EC) No. 1069/2009 indicates that approximately 35% of the theoretical substrate base is currently compliant for use in insect rearing for animal feed, representing the practically realisable fraction of the identified bioconversion potential. The study identifies key nutritional compatibility constraints between waste stream composition and insect species requirements, highlighting the importance of substrate blending for efficient bioconversion. These findings provide a spatially explicit foundation for planning circular bioeconomy strategies integrating waste management and sustainable insect protein production in Slovakia.