In a phenotypic screen of plants constitutively overexpressing DOF (DNA-binding-with-one-finger) transcription factors under the control of the Cauliflower mosaic virus 35S promoter, AtDOF4;2 was identified as a gene inducing a bushy plant phenotype and potentially being involved in the regulation of phenylpropanoid metabolism in Arabidopsis. Further molecular and biochemical characterization was performed in parallel using transgenic plants with enhanced and reduced AtDOF4;2 expression. The expression pattern of AtDOF4;2 was determined by quantitative real-time polymerase chain reaction (Q-RTPCR) and through promoter-beta-glucuronidase (GUS) fusions, indicating preferential transcriptional activity in axillary buds of the flower stalk, the hypocotyls periderm and in tapetum cells. Constitutive overexpression and RNAi-mediated silencing of AtDOF4;2 caused reciprocal changes in the expression of flavonoid biosynthetic genes and the accumulation of flavonoids under cold and high-light conditions. Moreover, tapetum-specific overexpression of AtDOF4;2 led to pollen grains devoid of flavonols. In contrast to its negative influence on flavonoid biosynthesis and coincident with high expression in the periderm and tapetum, AtDOF4;2 positively influences the production of hydroxycinnamic acids in the hypocotyl and flower buds, implicating its possible importance for suberin and sporopollenin production. These data provide evidence that AtDOF4;2, influences phenylpropanoid metabolism in an environmental and tissue-specific manner.