Intrinsically disordered (ID) regions, the regions that lack a well-defined three-dimensional structure under physiological conditions, are preferentially located in the cytoplasmic segments of plasma membrane proteins, many of which are known to be involved in cell signaling. This is in line with our studies that demonstrated that cytoplasmic domains of signaling subunits of immune receptors, including those of ζ, CD3ε, CD3δ and CD3γ chains of T cell receptor, Igα and Igβ chains of B cell receptor as well as the Fc receptor γ chain represent a novel class of ID proteins (IDPs). The domains all have one or more copies of an immunoreceptor tyrosine-based activation motif, tyrosine residues of which are phosphorylated upon receptor engagement in an early and obligatory event in the signaling cascade. Our studies of these IDPs revealed several unusual biophysical phenomena, including (1) the specific dimerization of disordered protein molecules, (2) the fast and slow dimerization equilibrium, depending on the protein, (3) no disorder-to-order transition and the lack of significant chemical shift and peak intensity changes upon dimerization or interaction with a well-folded partner protein and (4) the dual mode of binding to model membranes (with and without folding), depending on the lipid bilayer stability. Here, I highlight several of these studies that not only facilitate a rethinking process of the fundamental paradigms in protein biophysics but also open new perspectives on the molecular mechanisms involved in receptor signaling.