To improve water and nutrient acquisition from the soil, plants can modulate their root system architecture. Despite the importance of changes in root architecture to exploit local nutrient patches occurring in heterogenous soils or after placed fertilization, mechanisms integrating external nutrient signals into the root developmental programme remain poorly understood. Here, we show that local ammonium supply stimulates the accumulation of shoot-derived auxin in the root vasculature and promotes lateral root emergence to build a highly branched root system. Activities of pH and auxin reporters indicate that ammonium uptake mediated by ammonium transporters acidifies the root apoplast, which increases pH-dependent import of protonated auxin into cortical and epidermal cells overlaying lateral root primordia, and subsequently promotes their emergence from the parental root. Thereby, ammonium-induced and H+-ATPase-mediated acidification of the apoplast allows auxin to bypass the auxin importers AUX1 and LAX3. In nitrogen-deficient plants, auxin also accumulates in the root vasculature but a more alkaline apoplast leads to retention of auxin in these tissues and prevents lateral root formation. Our study highlights the impact of externally available nitrogen forms on pH-dependent radial auxin mobility and its regulatory function in organ development.