Protein secretion in eukaryotic cells begins with COPII-mediated transport from the endoplasmic reticulum (ER). The COPII coat assembles on the cytoplasmic side of the ER membrane in consecutive stages. The inner coat comprises the Sar1-Sec23/Sec24 heterotrimeric complex and is recruited through the activation of the Sar1 GTPase. Sar1 regulates the assembly/disassembly cycle of the coat, Sec23 acts as its GTPase activating protein (GAP), whereas Sec24 is involved in selecting cargo. The cage-forming Sec13/Sec31 outer coat is recruited by Sec23 to deform the membrane and allow budding of the cargo-loaded vesicle. My work provides evidence that the essential connection between the two coat layers is established by multiple different interfaces between Sec23 and the Sec31 disordered proline-rich domain. The Sec31 unstructured domain comprises known Sec23 binding sites, namely the ‘active fragment’ and short PPP motifs. My data demonstrate that although these interfaces are important for the inner/outer layer interaction, they are individually dispensable. This highlighted the existence of another previously undefined interface that uses an electrostatic interaction between net positively charged clusters of the Sec31 disordered domain and a negatively charged patch on the membrane-distal surface of Sec23. My work further reveals that PPP motifs and positively charged clusters within a disordered region could maintain the inner/outer coat interface irrespective of the underlying sequence. Moreover, my experiments suggest that in the regulatory protein Sec16, which also contains disordered domains, similar features have been adapted to prime COPII components for vesicle formation and to regulate their assembly. Lastly, I demonstrate that the Golgi-localised tether Grh1 can compete with Sec31 using similar disordered domain features to potentially stimulate uncoating and thus permit membrane fusion. An interface generated through multiple transient interactions highlights the capacity for their utilisation by sequence-divergent proteins to compete with the coat components during coat regulation, or to achieve its efficient disassembly. The proposed type of combinatorial interface explains how a stable structure can form robustly enough to generate vesicular carriers from a protein rich membrane, but also remain permissive to modifications and able to be easily disassembled in the appropriate context.