Background: Despite the limited successes of recent amyloid-targetting biologics, the need for a new pathogenesis mechanistic model of Alzheimer’s disease (AD) is a continuing priority, to facilitate improved rational drug design. Methods: To devise a new AD model, we performed an extensive, comprehensive series of in silico, in vitro, and in vivo studies explicitly evaluating the atomistic–molecular mechanisms of cytokine-mediated and amyloid-beta (Aβ)-mediated neurotoxicities in AD. Results: A new model of AD has been devised: In response to pathogen-/damage-associated molecular pattern-stimulating events (e.g., infection, trauma, ischaemia), Aβ is released as an early responder cytokine triggering an innate immunity cascade in which Aβ exhibits immunomodulatory/antimicrobial duality. However, Aβ’s antimicrobial properties result in a misdirected cytotoxic attack upon “self” neurons, arising from the electrophysiological similarities between neurons and bacteria in terms of transmembrane potential and anionic charges on outer membrane macromolecules. The subsequent breakdown products (amyloid-ganglioside complexes) released from the damaged neurons diffuse to adjacent neurons eliciting further release of Aβ, leading to a chronic, self-perpetuating disease cycle. In short, AD occurs because Aβ cannot differentiate neurons from bacteria. Conclusions: An innovative new model of AD has been devised, recognizing Aβ as a physiologically oligomerizing cytokine and conceptualizing AD as brain-centric autoimmune disorder of innate immunity.