Stomata are epidermal pores that control gas exchange between plants and the atmosphere. In Arabidopsis the ERECTA family (ERECTAf) receptors including ERECTA ERECTA-LIKE 1 (ERL1) and ERL2 redundantly play pivotal roles in enforcing the ‘one-cell-spacing’ rule. Accumulating evidence has demonstrated that the functional specificities of receptors are likely associated with their differential subcellular dynamics. The endoplasmic reticulum (ER)-resident chaperone complex SDF2-ERdj3B-BiP functions in many aspects of plant development. We employed pharmacological treatments combined with cell biological and biochemical approaches to demonstrate that the abundance of ERECTA was reduced in the erdj3b-1 mutant but the localization and dynamics of ERECTA were not noticeably affected. By contrast the erdj3b mutation caused the retention of ERL1/ERL2 in the ER. Furthermore we found that the function of SDF2-ERdj3B-BiP is implicated with the distinct roles of ERECTAf receptors. Our findings establish that the ERECTAf receptor-mediated signaling in stomatal development is ensured by the activities of the ER quality control system which preferentially maintains the protein abundance of ERECTA and proper subcellular dynamics of ERL1/ERL2 prior to the receptors reaching their destination – the plasma membrane – to execute their functions.