Nitrogen is an essential element for all life processes in plants. As such, plant roots dynamically respond to nitrogen availability below-ground by executing a signaling and transcriptional cascade resulting in altered plant growth, optimized for nutrient uptake. The NIN-LIKE PROTEIN 7 (NLP7) transcription factor senses nitrogen and along with its closely related paralog NLP6, coordinates these transcriptional responses. Here, we dissect a sub-circuit of the Arabidopsis nitrogen transcriptional network comprising AUXIN RESPONSE FACTOR 18 (ARF18), ARF9, DEHYDRATION RESPONSE ELEMENT BINDING-PROTEIN 26 (DREB26), A NAC-DOMAIN CONTAINING PROTEIN 032 (ANAC032), NLP6 and NLP7 transcription factors and their regulation of NITRATE REDUCTASE 1 (NIR1). Thecis-regulatory architecture of these factors are defined as well as their direct transcriptional regulation and demonstrate a network with multiple multi-node feedforward loops. Conservation and divergence of this network is similarly assessed inSolanum lycopersicum. The resulting network models are validated by measuring the transcriptional output of the network with the syntheticNITRATE-REGULATED PROMOTERin varying concentrations of available nitrogen revealing rewiring of nitrogen regulation across distinct plant lineages.