NaD1, a plant defensin isolated from the flowers of Nicotiana alata, is a cationic antimicrobial peptide (CAP) that displays potent antifungal activity against a variety of pathogenic fungi and tumor cells by attacking cell membranes. Specific interactions between NaD1 and phosphatidylinositol 4,5-bisphosphate (PI(4,5)P2), as well as NaD1 and phosphatidic acid (PA), have been revealed to trigger the assembly of NaD1-lipid oligomers that damage cell membranes. In this study, to comprehensively understand NaD1's interactions with diverse membrane phospholipids and their collective impact on membrane architecture, coarse-grained (CG) self-assembly molecular dynamics (MD) simulations and all-atom MD simulations were conducted to investigate interactions of NaD1 oligomeric states (monomer, dimer, and tetramer) with a Candida albicans membrane model containing physiological phospholipid compositions (POPC/POPE/POPI/POPS/POPG/POPA/DPP2 = 40:27:18:7:1:6:1 molar ratio) using GROMACS with Martini and charmm36m force fields. The results showed that phospholipids spontaneously formed bilayer structures with the NaD1 oligomer bound to their surfaces. The NaD1 monomer adopted two distinct binding orientations on the membrane, whereas both the dimer and tetramer adopted a single identical orientation. NaD1 exhibited strongest interfacial binding to DPP2 (model PIP2) and POPI, moderate affinity for POPE/POPC/POPS/POPA, and negligible interaction with POPG. Further calculation showed interface phospholipid redistribution following NaD1 binding, which featured increased DPP2/POPI/POPA and decreased POPC/POPE/POPS/total phospholipids versus NaD1-free membranes, quantitatively showing the perturbation of NaD1 on the membrane structure, together with the membrane thickness reduction and area per lipid (APL) increase (from monomer system, dimer system, to tetramer system) revealed by fundamental bilayer property analysis. These results revealed the "carpet-like" mechanism of NaD1 on C. albicans cell membranes at low NaD1/lipid ratios. In addition, this study also revealed the key binding sites of DPP2 (Lys4, His33, Ser35-Leu38, and Arg40, reproducing the hydrogen-bond network in the crystal structure), the contribution of POPI (besides DPP2) to NaD1 dimerization, and the role of POPE and POPS (besides POPA) in promoting "side-by-side" NaD1 tetramer formation. The spontaneous formation of NaD1 "head-to-head" tetramers was observed for the first time, providing new insights into the process of NaD1 "carpet-like" structure formation. Overall, the molecular details in this study provide us a better understanding of the "carpet-like" model of the NaD1 antimicrobial mechanism.