Autophagy is an essential catabolic cellular homeostasis process conserved in all eukaryotes. BECN1, a key autophagy protein involved in autophagosome nucleation, comprises of a large, poorly conserved, N-terminal intrinsically disordered region (IDR); a flexible helical domain; a coiled-coil domain (CCD) that forms anti-parallel homodimers in the absence of other interacting partners; and a β-α repeated autophagy specific domain (BARAD). The IDR of higher eukaryotes includes a BCL2 homology 3 domain (BH3D), which undergoes dramatic disorder-to-helix transitions upon binding to anti-apoptotic and anti-autophagic BCL2s. We show that the BH3D is not required for starvation-induced autophagy upregulation suggesting that BCL2-binding to the BH3D does not directly impede a pro-autophagy function of the BH3D, rather it may impact structure, oligomerization, interactions and function of other BECN1 domains. CCD C-terminal residues, named the overlap helix (OH), pack in two mutually-exclusive states stabilized by the same interface residues: against either the partner helix in a CCD dimer or the BARAD. We show that mutation of these interface residues abrogates starvation-induced autophagy upregulation. Together with our complementary structural studies, this suggests that autophagy-inactive BECN1 adopts conformations preventing the BARAD from membrane-association, with BECN1 heterodimerization with ATG14 or UVRAG disrupting this inhibitory conformation. In the BECN1 homodimer, the OH packs against a nuclear export signal sequence (NES) at the N-terminus of the partner CCD. We show that when released from this interaction, the NES can interact with the complex of the nuclear exporter, Chromosomal Region Maintenance 1 protein and a GTP-bound small G-protein, Ran. This interaction is essential for BECN1 export to the cytoplasm, and for autophagy. Two invariant CxxC motifs bookend the IDR. We find that both CxxC motifs are required, but the intervening IDR is less important, for starvation-triggered upregulation of autophagy. We demonstrate that BECN1 binds Zn2+ in a 1:1 molar ratio. Further, mutation of the invariant cysteines or treatment with reducing agent abrogates Zn2+ co-ordination, demonstrating that the invariant CxxC motifs are responsible for binding Zn2+. We use diverse biophysical methods to show that Zn2+-binding impacts the conformation and structural transitions of the BECN1 IDR, thereby playing an important role in regulating autophagy.