Transition metals directly contribute to the neurotoxicity of the aggregates of the amyloid-forming Aβ peptide. The understanding and rationalization of the coordination modes of metals to Aβ amyloid is, therefore, of paramount importance to understand the capacity of a given metal to promote peptide aggregation. Experimentally, multiple Aβ-metal structures have been resolved, which exhibit different modes of coordination in both the monomeric and oligomeric forms of Aβ. Although Zn(II) metalloproteins are very abundant and often involve cysteine residues in the first coordination shell, in the case of Aβ-Zn(II), though, Zn(II) is coordinated by glutamic/aspartic acid and/or histidine residues exclusively, making for an interesting case study. Here we present a systematic analysis of the underlying chemistry on Aβ-Zn(II) coordination, where relative stabilities of different coordination arrangements indicate that a mixture of Glu/Asp and His residues is favored. A detailed comparison between different coordination shell geometries shows that tetrahedral coordination is generally favored in the aqueous phase. Our calculations show an interplay between dative covalent interactions and electrostatics which explains the observed trends. Multiple structures deposited in the Protein Data Bank support our findings, suggesting that the trends found in our work may be transferable to other Zn(II) metalloproteins with this type of coordination.