Proteins in solution continually fluctuate between conformational states, and these dynamics play a central role in their structural and colloidal stability. Using molecular dynamics simulations, we show that insulin exists as a conformational ensemble in solution, which can be quantitatively described using a Markov state model. This analysis resolves the two slowest motions of the insulin monomer: unfolding of the A3(Val)-A6(Cys) region and a side-chain rotation of B4(Gln). We further demonstrate that the ionic liquid choline dihydrogen phosphate (CDHP) stabilizes insulin by reducing the population of partially unfolded states formed via unraveling of the A1-A6 α-helix. This effect is supported experimentally, where CDHP also increased insulin's resistance to aggregation. Simulations suggest that the stabilization is primarily driven by the dihydrogen phosphate anion, which preferentially interacts with residues in proximity to the unfolding hotspot. Together, this study demonstrates how modulating the conformational ensemble may directly improve protein stability and mitigate protein aggregation.