SummaryATAF1is a member of a largely uncharacterized plant‐specific gene family encoding NAC transcription factors, and is induced in response to various abiotic and biotic stimuli inArabidopsis thaliana. Previously, we showed that a mutant allele ofATAF1compromises penetration resistance in Arabidopsis with respect to the non‐host biotrophic pathogenBlumeria graminisf. sp.hordei(Bgh). In this study, we have used genome‐wide transcript profiling to characterize signalling perturbations inataf1plants followingBghinoculation. Comparative transcriptomic analyses identified an over‐representation of abscisic acid (ABA)‐responsive genes, including the ABA biosynthesis geneAAO3, which is significantly induced inataf1plants compared to wild‐type plants following inoculation withBgh. Additionally, we show thatBghinoculation results in decreased endogenous ABA levels in anATAF1‐dependent manner, and that the ABA biosynthetic mutantaao3showed increased penetration resistance toBghcompared to wild‐type plants. Furthermore, we show thatataf1plants show ABA‐hyposensitive phenotypes during seedling development and germination. Our data support a negative correlation between ABA levels and penetration resistance, and identify ATAF1 as a new stimuli‐dependent attenuator of ABA signalling for the mediation of efficient penetration resistance in Arabidopsis uponBghattack.