α-Synuclein is an intrinsically disordered protein with a critical role in the development of many neurodegenerative diseases including Parkinson's disease. The aggregation processes leading to its pathogenicity as well as many of its putative physiological roles are greatly influenced by its dynamic and modular membrane binding capabilities. Upon binding, under normal physiological conditions, α-Synuclein shows distinct levels of structure formation along its sequence with varying levels of association with the lipid membrane. Dynamic properties at the interphase of membrane association are key for understanding α-Synuclein's physiological and pathological roles and is therefore of chief interest. In this thesis, I develop various coarse-grained molecular dynamics (CG-MD) models to study the contribution of order and disorder to the modular and dynamic membrane interaction of the different regions of α-Synuclein. The CG-MD membrane binding assays, and population models here presented have allowed the observation of the conformational specific contributions towards membrane binding of the different regions of α-Synuclein. The residue specific resolution of these assays resulted in a better understanding of the N-terminal anchor and central region binding mechanisms. A better understanding of the initiation and stabilisation of the N-terminal was achieved through the study of key mutations in the region, with membrane binding assays. A combination of membrane binding assays and NMR-driven population studies revealed the potentially faster dynamics of the binding of the central region, allowing for a kinetically more favourable double anchor mechanism, involved in synaptic vesicle clustering at synaptic terminals.