As a major determinant of the nutrient-acquiring root surface, root hairs (RHs) provide a low-input strategy to enhance nutrient uptake. Although primary and lateral roots exhibit elongation responses under mild nitrogen (N) deficiency, the foraging response of RHs and underlying regulatory mechanisms remain elusive. Employing transcriptomics and functional studies revealed a framework of molecular components composing a cascade of auxin synthesis, transport, and signaling that triggers RH elongation for N acquisition. Through upregulation of Tryptophan Aminotransferase of Arabidopsis 1 (TAA1) and YUCCA8, low N increases auxin accumulation in the root apex. Auxin is then directed to the RH differentiation zone via the auxin transport machinery, AUXIN TRANSPORTER PROTEIN 1 (AUX1) and PIN-FORMED 2 (PIN2). Upon arrival to the RH zone, auxin activates the transcription factors AUXIN RESPONSE FACTOR 6 and 8 (ARF6/8) to promote the epidermal and auxin-inducible transcriptional module ROOT HAIR DEFECTIVE 6 (RHD6)-LOTUS JAPONICA ROOT HAIRLESS-LIKE 3 (LRL3) to steer RH elongation in response to low N. Our study uncovers a spatially defined regulatory signaling cascade for N foraging by RHs, expanding the mechanistic framework of hormone-regulated nutrient sensing in plant roots.