αS-Casein, the major milk protein, comprises αS1- and αS2-casein and acts as a molecular chaperone, stabilizing an array of stressed target proteins against precipitation. Here, we report that αS-casein acts in a similar manner to the unrelated small heat-shock proteins (sHsps) and clusterin in that it does not preserve the activity of stressed target enzymes. However, in contrast to sHsps and clusterin, α-casein does not bind target proteins in a state that facilitates refolding by Hsp70. αS-Casein was also separated into α- and α-casein, and the chaperone abilities of each of these proteins were assessed with amorphously aggregating and fibril-forming target proteins. Under reduction stress, all α-casein species exhibited similar chaperone ability, whereas under heat stress, α-casein was a poorer chaperone. Conversely, αS2-casein was less effective at preventing fibril formation by modified κ-casein, whereas α- and αS1-casein were comparably potent inhibitors. In the presence of added salt and heat stress, αS1-, α- and αS-casein were all significantly less effective. We conclude that αS1- and α-casein stabilise each other to facilitate optimal chaperone activity of αS-casein. This work highlights the interdependency of casein proteins for their structural stability.