Plant cells are encased in a semi-rigid cell wall of complex build. As a consequence, cell wall remodeling is essential for the control of growth and development as well as the regulation of abiotic and biotic stress responses. Plant cells actively sense physico-chemical changes in the cell wall and initiate corresponding cellular responses. However, the underlying cell wall monitoring mechanisms remain poorly understood. In Arabidopsis the atypical receptor kinase STRUBBELIG (SUB) mediates tissue morphogenesis. Here, we show that SUB-mediated signal transduction also regulates the cellular response to a reduction in the biosynthesis of cellulose, a central carbohydrate component of the cell wall. SUB signaling affects early increase of intracellular reactive oxygen species, stress gene induction as well as ectopic lignin and callose accumulation upon exogenous application of the cellulose biosynthesis inhibitor isoxaben. Moreover, our data reveal that SUB signaling is required for maintaining cell size and shape of root epidermal cells and the recovery of root growth after transient exposure to isoxaben. SUB is also required for root growth arrest in mutants with defective cellulose biosynthesis. Genetic data further indicate that SUB controls the isoxaben-induced cell wall stress response independently from other known receptor kinase genes mediating this response, such as THESEUS1 or MIK2. We propose that SUB functions in a least two distinct biological processes: the control of tissue morphogenesis and the response to cell wall damage. Taken together, our results reveal a novel signal transduction pathway that contributes to the molecular framework underlying cell wall integrity signaling.