Mycotoxins are widely consumed food contaminants. Mechanistic studies support potential carcinogenic effects of mycotoxins in the human intestine, yet no studies have investigated these associations in population-based settings. This study aimed to investigate associations between dietary mycotoxin exposures and colorectal cancer risk. Dietary questionnaire data from the European Prospective Investigation into Cancer and Nutrition (EPIC) were combined with mycotoxin food occurrence data from the European Food Safety Authority (EFSA). Associations between mycotoxin exposures and colorectal cancer (CRC) risk and its anatomical sub-sites were evaluated in multivariable Cox proportional hazards regression models to compute hazard ratios (HR) and their 95% confidence intervals (CI), accounting for potential confounders. Food groups that explained the greatest variation in mycotoxin intakes were cereal-based products, vegetables, non-alcoholic beverages and fruits. For individual mycotoxins, deoxynivalenol (DON) was positively associated with CRC risk (HR top vs. bottom tertiles [T3vsT1] = 1.14; 1.04–1.24), while patulin (PAT) was positively associated with rectal cancer risk only (HR^T3vsT1 = 1.18; 1.05–1.32). Sensitivity analyses indicated differential results for men versus women with significant positive associations for DON and CRC risk found only in men. In conclusion, dietary mycotoxin exposures may be related to higher CRC risk. Further investigation in independent cohorts and through mechanistic studies is warranted.