During the transition from seed to seedling, emerging embryos strategically balance the available resources between building up defenses against environmental threats, and initiating the developmental program that promotes the switch to autotrophy. We present evidence of a critical role for the phenylalanine (Phe) biosynthetic activity of AROGENATE DEHYDRATASE 3 (ADT3) in coordinating ROS homeostasis and cotyledon development in etiolated Arabidopsis thaliana seedlings. We show that ADT3 is expressed in the cotyledon and shoot apical meristem, mainly in the cytosol, and the epidermis of adt3 cotyledons contains high levels of reactive oxygen species (ROS). Genome-wide proteomics ofadt3 mutant revealed a general downregulation of plastidic proteins and ROS scavenging enzymes, corroborating the hypothesis that ADT3 supply of Phe is required to control of ROS concentration and distribution to protect cellular components. In addition, loss of ADT3 disrupts cotyledon epidermal patterning by affecting the number and expansion of pavement cells and stomata cell fate specification; we also observed severe alterations in mesophyll cells, which lack oil bodies and normal plastids. Interestingly, upregulation of the pathway leading to cuticle production is accompanied by an abnormal cuticle structure and/or deposition in the adt3 mutant. Such impairment results in an increase in cell permeability and provides a link to understand the cell defects in the adt3 cotyledon epidermis. We suggest an additional role of Phe in supplying nutrients to the young seedling.