Dioxins are highly toxic persistent organic pollutants bioaccumulated by both plants and animals that cause severe developmental abnormalities in humans. We investigated the effects of dioxins on seed development in Arabidopsis. Plants were exposed to various concentrations of the most toxic congener of dioxins, 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) and the effects on seed development were analysed in-depth at transcriptome, proteome and metabolome levels. Exposure to dioxin led to generalized effects on vegetative tissues plus a specific set of perturbations to seed development. Mature seeds from TCDD-treated plants had a characteristic 'wrinkled' phenotype, due to a two-thirds reduction in storage oil content. Transcriptional analysis of a panel of genes related to lipid and carbohydrate metabolism was consistent with the observed biochemical phenotypes. There were increases in WRI1 and LEC1 expression but decreases in ABI3 and FUS3 expression, which is puzzling in view of the low seed oil phenotype. This anomaly was explained by increased expression of 20S proteasome components that resulted in a substantial degradation of WRI1 protein, despite the up-regulation of the WRI1 gene. Our findings reveal novel effects of dioxins that lead to altered gene regulation patterns that profoundly affect seed development in Arabidopsis.