Plasma membrane-resident receptor kinases (RKs) initiate signalling pathways important for plant immunity and development. In Arabidopsis thaliana, the receptor for the elicitor-active peptide epitope of bacterial flagellin, flg22, is encoded by FLS2, which promotes plant immunity. Despite its relevance, the molecular components regulating the FLS2-mediated signalling remain largely unknown. We show that the plasma membrane calcium (Ca2+) ATPase ACA8 forms a complex with FLS2 in planta. ACA8 and its closest homologue ACA10 are required for limiting the growth of virulent bacteria. One of the earliest flg22 responses is the transient increase of cytosolic Ca2+ ions, which is crucial for many of the well-described downstream responses, e.g. generation of reactive oxygen species (ROS) and the transcriptional activation of defence-associated genes. Mutant aca8 aca10 plants show decreased flg22-induced Ca2+ and ROS bursts, and exhibit altered transcriptional reprogramming. In particular, mitogen-activated protein kinase (MAPK)-dependent flg22-induced gene expression is elevated, while calcium-dependent protein kinase (CDPK)-dependent flg22-induced gene expression is reduced. These results demonstrate that the fine regulation of Ca2+ fluxes across the plasma membrane is critical for the coordination of the downstream MAMP responses and suggest a mechanistic link between the FLS2 receptor complex and signalling kinases via the secondary messenger Ca2+. ACA8 also interacts with other RKs such as BRI1 and CLV1 known to regulate plant development, and both aca8 and aca10 mutants show morphological phenotypes, suggesting additional roles for ACA8 and ACA10 in developmental processes. Thus, Ca2+ ATPases appear to represent general regulatory components of RK-mediated signalling pathways.