1. Seed longevity, the maintenance of viability during dry storage, is a crucial factor to preserve plant genetic resources and seed vigor. Inference of a temporal gene-regulatory network of seed maturation identified auxin signaling as a putative mechanism to induce longevity-related genes. 2. Using auxin-response sensors and tryptophan-dependent auxin biosynthesis mutants of Arabidopsis thaliana L., the role of auxin signaling in longevity was studied during seed maturation. 3. DII and DR5 sensors demonstrated that concomitant with the acquisition of longevity, auxin signaling input and output increased and underwent a spatio-temporal redistribution, spreading throughout the embryo. Longevity of seeds of single auxin biosynthesis mutants with altered auxin signaling activity was affected in a dose-response manner depending on the level of auxin activity. Longevity-associated genes with promoters enriched in auxin response elements and the master regulator ABSCISIC ACID INSENSITIVE 3 were induced by auxin in developing embryos and deregulated in auxin biosynthesis mutants. The beneficial effect of exogenous auxin during seed maturation on seed longevity was abolished in abi3-1 mutants. 4. These data suggest a role for auxin signaling activity in the acquisition of longevity during seed maturation.