Light is an environmental signal that modulates plant defenses against attackers. Recent research has focused on the effects of light on defense hormone signaling; however, the connections between light signaling pathways and the biosynthesis of specialized metabolites involved in plant defense have been relatively unexplored. Here, we show thatArabidopsisBBX29, a protein that belongs to the B-Box transcription factor (TF) family, integrates photomorphogenic signaling with defense responses by promoting flavonoid, sinapate and glucosinolate accumulation inArabidopsisleaves.AtBBX29transcript levels were up regulated by light, through photoreceptor signaling pathways. Genetic evidence indicated that AtBBX29 up-regulatesMYB12gene expression, a TF known to induce genes related to flavonoid biosynthesis in a light-dependent manner, andMYB34andMYB51, which encode TFs involved in the regulation of glucosinolate biosynthesis. Thus,bbx29knockout mutants displayed low expression levels of key genes of the flavonoid biosynthetic pathway, and the opposite was true inBBX29overexpression lines. In agreement with the transcriptomic data,bbx29mutant plants accumulated lower levels of kaempferol glucosides, sinapoyl malate, indol-3-ylmethyl glucosinolate (I3M), 4-methylsulfinylbutyl glucosinolate (4MSOB) and 3-methylthiopropyl glucosinolate (3MSP) in rosette leaves compared to the wild-type, and showed increased susceptibility to the necrotrophic fungusBotrytis cinereaand to the herbivoreSpodoptera frugiperda. In contrast,BBX29overexpressing plants displayed increased resistance to both attackers. In addition, we found that AtBBX29 plays an important role in mediating the effects of ultraviolet-B (UV-B) radiation on plant defense againstB. cinerea. Taken together, these results suggest that AtBBX29 orchestrates the accumulation of specific light-induced metabolites and regulatesArabidopsisresistance against pathogens and herbivores.Graphical AbstractSupplementary InformationThe online version contains supplementary material available at 10.1007/s43630-023-00391-8.