The fibrillar aggregation of the intrinsically disordered protein α-synuclein is a characteristic hallmark of Parkinson’s disease (PD). Molecular chaperones are a diverse family of proteins responsible for the maintenance of protein homoeostasis. The small heat-shock protein (sHsp) chaperones, αB-crystallin and Hsp27, have been shown to bind stably to α-synuclein fibrils and inhibit their elongation; alternatively, the Hsp70 system of chaperones have been shown to disaggregate mature α-synuclein fibrils. However, most studies that investigate the dynamics of α-synuclein fibril disaggregation by the Hsp70 system have done so in the absence of sHsps and/or monomeric α-synuclein, which exists at high concentrations in the neurons affected by PD. To address this, we performed thioflavin-T (ThT)-based assays to assess the ability of sHsps to assist in the Hsp70-mediated disaggregation of α-synuclein fibrils in the presence of aggregation-prone α-synuclein monomers. Increasing concentrations of monomeric α-synuclein reduces the magnitude of chaperone-mediated disaggregation, where the elongation of α-synuclein fibrils is favoured over chaperone-mediated disaggregation. This suggests that the Hsp70 system chaperones are unable to meaningfully disassemble pre-formed fibrils when monomeric α-synuclein is present. Additionally, we report that the addition of sHsps does not improve the disaggregation reaction (implying no cooperative action between these chaperone systems) but instead functions to inhibit further fibril elongation. Overall, these results demonstrate how the molecular chaperone disaggregation machinery can become easily overwhelmed by even modest elongation kinetics, resulting in proteostasis failure that likely contributes to the development of neurodegenerative diseases.