COPII coated vesicles mediate export from the endoplasmic reticulum (ER). Their fusion is thought to generate the intermediate compartment (IC/ERGIC). Two mutually exclusive models explain the biogenesis of the ERGIC: the stationary hypothesis and the maturation hypothesis. The stationary hypothesis considers the ERGIC a stable compartment, into which vesicles enter and exit, and therefore predicts the existence of a specific ERGIC-export motif. Here, we identify such a motif in C-terminus of the GABA-transporter-1 (GAT1): ER-export of GAT1 is contingent on the binding of Sec24 to the C-terminus of GAT1 (i.e. to 566RL567). However, after reaching the ERGIC, trafficking of GAT1 becomes dependent on a distinct, tri- hydrophobic motif in the C-terminus (569VMI571). Thus, our observations show for the first time that export of a protein from the ERGIC is dependent on amino acid residues provided by the cargo molecule.