Growing evidence suggests transmission of colorectal cancer risk through the maternal line. There is scant information about transmission through the paternal line, despite plausible evidence from mammal experiments. We examined the association between paternal occupation and colorectal cancer in the Child Health and Development Studies, a multi-generational cohort followed for 60 years. Pregnant mothers completed in-person interviews at enrollment (1959-1966) and reported demographic and health-related information for her and her husband, including occupation. Colorectal cancer in adult (age ≥18 years) offspring was ascertained from a population-based cancer registry. Cox proportional hazards models were used to estimate adjusted hazard ratios (aHR), with follow-up accrued from birth through cancer diagnosis, death, or last contact. Paternal occupations included: 37.0% professional, technical, or managerial; 13.7% clerical or sales; 30.5% crafts or operative; and 17.5% service work or labor. Over 716,133.5 person-years of follow-up, 79 offspring were diagnosed with colorectal cancer (median age at diagnosis: 50 years [range: 23-59 years]). Offspring of fathers employed in crafts, operative, service, or labor occupations had higher incidence rates of colorectal cancer (15.66 per 100,000 person-years; 95% CI 11.47, 20.89) compared to professional, technical, or managerial occupations (6.84 per 100,000 person-years; 95% CI 3.73, 11.47). Risk associated with these occupations remained elevated after adjustment for maternal race, paternal education, and offspring year of birth (aHR 1.99; 95% CI 1.03, 3.87). Our findings support possible transmission of cancer risk through the paternal line.