Research to control yield losses from Sclerotinia (Sclerotinia sclerotiorum) in oilseed rape (Brassica napus) has focused on stem resistance. However, resistance to leaf infection against this pathogen would also be beneficial, both in limiting additional plant leaf damage and in reducing inoculum build up within-crop and resultant spread onto stems. Three B. napus breeding populations, C2 (NC-8 × RQ-001-NCA-8 NC2-7), C5 (cv. Charlton × RQ-001-NCA-8 NC2-7) and C6 (cv. Charlton × NC4-5), were screened for leaf resistance (based on mean lesion diameter) under controlled environment conditions. Each population consisted of parents (P1 and P2), F1, F2, BC1P1 and BC2P2, except for C5 that lacked BC1P1. Moderate broad sense heritability for leaf resistance (0.45) to S. sclerotiorum was only found in population C6, where genetic variance was mostly non-additive. Analyses of generation means and variances indicated that both dominance and complex epistatic interactions were present in C6. Bivariate analysis revealed a positive genetic covariance between the non-additive effects for mean leaf lesion and cotyledon lesion diameters, and significant negative covariance of residuals, which supports a common genetic control of cotyledon and leaf resistance to S. sclerotiorum. These results will guide breeders in selection and development of genotypes with both cotyledon and leaf resistance against this important pathogen worldwide.