Astrocytes play an active role in shaping and maintaining neuronal circuits and the blood-brain barrier. In addition to their long-established role in extracellular potassium buffering and glutamate uptake, these cells can also regulate the activity of local synaptic circuits through secretion and clearance of neurotransmitters. Whilst the molecular signal exchange between astroglia and synapses occurs in a highly heterogeneous microenvironment on the nanoscale, the spatial subcellular distribution of the underlying molecular machineries remains poorly understood. Similarly, in addition to closely associating with excitatory synapses throughout the brain, astrocytes also ensheath blood vessels as part of the blood-brain barrier. Here, they regulate solute and fluid transport in and out of the brain through their end feet. The gross morphological architecture as well as the molecular composition of both astrocytic compartments, peri-synaptic astrocytic processes and end feet, change during normal physiological processes but especially in pathophysiology of all neurological diseases. We employed super-resolution single molecule localisation microscopy (SMLM) to visualise the 3D positions of neurotransmitter receptors and transporters in astrocytes. Using SMLM, we were able to localise cytoskeletal proteins as well as clusters of receptors and transporters in fixed cultured cells and brain slices. We assessed the positional relationship between synapses or blood vessels and astroglial receptors and transporters through multi-colour imaging. We determined that astroglial coverage of excitatory synapses and blood vessels is altered in different conditions compatible with long-term synaptic potentiation and depression as well as disease states, providing further evidence for the role of astrocytes in shaping synaptic transmission.