One of the mechanisms of δ cytotoxicity attributed to Alzheimer’s Aβ peptides postulates that their aggregation disrupts membrane structure causing uncontrollable permeation of Ca2+ ions. To gain molecular insights into these processes, we have performed all-atom explicit solvent replica exchange with solute tempering (REST) molecular dynamics simulations probing aggregation of the naturally occurring Aβ fragment Aβ25-35 within the DMPC lipid bilayer. To compare the impact produced on the lipid bilayer by Aβ25-35 oligomers and monomers, we used as a control our previous simulations, which explored binding of Aβ25-35 monomers to the same bilayer. We found that compared to monomeric species aggregation results in much deeper insertion of Aβ25-35 peptides in the hydrophobic core of the lipid bilayer causing more pronounced disruption in its structure. Our study indicates that Aβ25-35 peptides aggregate by incorporating monomer-like structures with stable C-terminal helix. As a result, the Aβ25-35 dimer features unusual helix head-to-tail topology supported by a parallel off-registry interface. The head-to-tail topology readily affords further growth of an aggregate by recruiting additional peptides. Free energy landscape of Aβ25-35 binding and aggregation reveals that inserted dimers represent the dominant equilibrium state augmented by two metastable states associated with surface bound dimers and inserted monomers. Analysis of the free energy landscape allows us to propose the pathway and mechanism of Aβ25-35 binding, aggregation, and insertion into the lipid bilayer. Our all-atom explicit solvent simulations provide the first, to our knowledge, all-atom description of equilibrium de novo Aβ peptide aggregation mediated by a lipid bilayer.