The plasma membrane (PM) is highly dynamic and undergoes extensive remodelling during regulated exocytosis and endocytosis. The PM is also spatially organised into distinct domains, including cortical endoplasmic reticulum (ER)-associated PM zones and ER-free PM zones. ER-PM contacts are recognised as important sites for non-vesicular calcium and membrane lipid transport, while exocytic and endocytic vesicular trafficking events are thought to take place exclusively in ER-free PM zones. These two PM domains have been considered to be functionally and spatially uncoupled. Our work is revealing vital roles for inter-organelle cross talk between the ER and PM in membrane trafficking pathways. We are addressing how the architecture of ER-PM contacts is regulated and how distinct ER-PM contacts govern PM domain organization and dynamics. We will present our recent findings on roles for membrane lipid dynamics taking place at ER-PM contacts in the control of phosphoinositide (PI) kinase regulatory networks during regulated exo- and endocytosis.