We investigate the relationship between the inherent secondary structure and aggregation propensity of peptides containing chameleon sequences (i.e., sequences that can adopt either alpha or beta structure depending on context) using a combination of replica exchange molecular dynamics simulations, ion-mobility mass spectrometry, circular dichroism, and transmission electron microscopy. We focus on an eight-residue long chameleon sequence that can adopt an alpha-helical structure in the context of the iron-binding protein from Bacillus anthracis (PDB id 1JIG) and a beta-strand in the context of the baculovirus P35 protein (PDB id 1P35). We show that the isolated chameleon sequence is intrinsically disordered, interconverting between alpha helical and beta-rich conformations. The inherent conformational plasticity of the sequence can be constrained by addition of flanking residues with a given secondary structure propensity. Intriguingly, we show that the chameleon sequence with helical flanking residues aggregates rapidly into fibrils, whereas the chameleon sequence with flanking residues that favor beta-conformations has weak aggregation propensity. This work sheds new insights into the possible role of alpha-helical intermediates in fibril formation.