Calcium ions (Ca2+) play pivotal roles in a host of cellular signalling processes. The requirement to maintain resting cytosolic Ca2+ levels in the 100–200 nM range provides a baseline for dynamic excursions from resting levels that determine the nature of many physiological responses to external stimuli and developmental processes. This review provides an overview of the key components of the Ca2+ homeostatic machinery, including known channel-mediated Ca2+ entry pathways along with transporters that act to shape the cytosolic Ca2+ signature. The relative roles of the vacuole and endoplasmic reticulum as sources or sinks for cytosolic Ca2+ are considered, highlighting significant gaps in our understanding. The components contributing to mitochondrial, chloroplast and nuclear Ca2+ homeostasis and organellar Ca2+ signals are also considered. Taken together, a complex picture of the cellular Ca2+ homeostatic machinery emerges with some clear differences from mechanisms operating in many animal cells.