Karrikins are abiotic plant growth regulators that promote seed germination and seedling photomorphogenesis. The receptor-enzyme KARRIKIN INSENSITIVE 2 (KAI2) initiates the karrikin perception and response pathway that depends on degradation of the putative transcriptional regulators SUPPRESSOR OF MAX2 1 (SMAX1) and SMAX1-LIKE 2 (SMXL2). However, transcriptional targets of KAI2-SMAX1-SMXL2 signalling are poorly defined. Here we describe a transcriptomic analysis of Arabidopsis thaliana seedlings following chemical induction of KAI2 expression and activation by karrikins. Among the upregulated genes is KAI2-DEPENDENT CYTOCHROME P450 1 (KDP1), an uncharacterised member of the CYP708 family that is unique to the Brassicaceae. In seedlings, KDP1 transcripts were upregulated by exogenous karrikins, downregulated in kai2 mutants, and upregulated in smax1 smxl2 double mutants. Loss-of-function kdp1mutants display increased sensitivity to salt stress, impaired photomorphogenesis, reduced responses to drought and phosphorous starvation, and early flowering. Constitutive overexpression of KDP1 was not tolerated. GC-MS analyses indicate that kdp1 mutants accumulate a metabolite with a previously undescribed fragmentation spectrum, consistent with a block in a biosynthetic pathway for a potentially novel compound. These results are consistent with KDP1 mediating some of the diverse downstream effects of KAI2-dependent signalling. Notably, KDP1 may represent a target for precise manipulation of agronomically important traits within brassica crops.