The epidermal cell layer and the tissues that lie underneath have different intrinsic functions during plant development. The stem cells within the shoot apical meristem (SAM) that give rise to aerial structures are located in the epidermal and internal tissue layers. However, our understanding of how the functions of these stem cells are coordinated across tissue layers so stem cells can behave as a single population remains limited. WUSCHEL (WUS) functions as a master regulator of stem cell activity. Here we show that loss of function in the ERECTA (ER)-family receptor kinase genes can rescue the mutant phenotype of wus plants (loss of stem cells), as demonstrated by the reinstated expression of a stem cell marker gene in the SAM epidermis. Localized ER expression in the epidermis can suppress the er-family SAM phenotype. Furthermore, the CLAVATA3- and cytokinin-induced outputs, which contribute to stem cell homeostasis, are dysfunctional in a tissue layer-specific manner in er-family mutants. Collectively, our findings suggest that the ER family plays a role in the coordination of stem cell behavior between different SAM tissue layers.