The plant hormone auxin is thought to provide positional information for the acquisition of cell identity during plant development. However information on auxin distribution at the cellular level and on mechanisms sensing auxin in space and time are still largely missing. The control of gene expression in response to auxin involves a complex network of over 50 potentially interacting transcriptional activators and repressors, the Aux/IAA and Auxin Response factors (ARF). Here we performed a large-scale analysis of the Aux/IAA-ARF pathway in the shoot apex, where dynamic auxin-based patterning control organogenesis. A comprehensive expression map and full interactome uncovered an unexpectedly simple distribution and structure of this pathway in the shoot apex. Using modelling, we predicted spatial differences in auxin sensitivity and strong buffering capacities of the Aux/IAA-ARF network. By combining a novel auxin signalling sensor reporting the input into the signalling pathway with the DR5 transcriptional output reporter, we were able to confirm these predictions. We thus show that the auxin signalling network is essential to create robust patterns at the shoot apex.