The endoplasmic reticulum (ER) is a large and highly dynamic component of the eukaryotic endomembrane system. In eukaryotic microalgae, it plays six distinct roles: (1) It envelopes the chromatin to form the nucleus. (2) It forms cisternae in the cytoplasm, some of which scaffold the synthesis of proteins destined for incorporation into membranes or for secretion. (3) It associates with Golgi cisternae to scaffold the synthesis of glycosylated proteins. (4) It associates with the plasma membrane to mediate the synthesis and secretion of hydrophobic molecules. (5) It mediates the synthesis of cytoplasmic lipid bodies. (6) In lineages harboring complex plastids of red algal ancestry, it forms the chloroplast ER, which envelops the primary chloroplast envelope. In this review, these systems are illustrated using the quick-freeze deep-etch electron microscopy (QFDEEM) technique, which lifts up the topological configurations adopted by this gossamer system. A key finding is that in all the complex microalgae examined except dinoflagellates, the inner nuclear envelope membrane associates directly with the plastid-contiguous membrane of the chloroplast ER at foci designated as chloroplast-nuclear junctions. These junctions may play a role in regulating the maintenance and physiology of the complex organelles.