The plasma membrane (PM) forms extensive close junctions with the cortical endoplasmic reticulum (cER) in many cell types, ranging from yeast to mammals. How cells modulate structural plasticity of ER-PM contacts to accommodate space-demanding cortical events is largely unknown. Here, we report a role for eisosome-driven PM furrows in regulating ER-PM contact plasticity in fission yeast. We demonstrate that eisosome-coated PM invaginations function to stabilize local ER-PM contacts and attenuate cER remodeling dynamics through electrostatic Scs2-Pil1 interactions. We also identify divergent roles of ER-shaping proteins in controlling cER remodeling capacity and ER-PM contact plasticity. Furthermore, we show that eisosome organization is responsive to PM tension variations during active PM remodeling, which may enable adaptive control of ER-PM contact plasticity to potentially coordinate with space-demanding PM events. We thus propose a cellular strategy of modulating membrane contact plasticity by deploying sensory elements at contact sites.