Linear motifs (LMs) are protein–protein interaction sites, typically consisting of ~4–20 amino acid residues that are often found in disordered proteins or regions, and function largely independent from other parts of the proteins they are found in. These short sequence patterns are involved in a wide spectrum of biological functions including cell cycle control, transcriptional regulation, enzymatic catalysis, cell signaling, protein trafficking, etc. Even though LMs may adopt defined structures in complexes with targets, which can be determined by conventional methods, their uncomplexed states can be highly dynamic and difficult to characterize. This hinders our understanding of the structure–function relationship of LMs. Here, the uncomplexed states of 6 different LMs are investigated using atomistic molecular dynamics (MD) simulations. The total simulation time was about 63 µs. The results show that LMs can have distinct conformational propensities, which often resemble their complexed state. As a result, the free state structure and dynamics of LMs may hold important clues regarding binding mechanisms, affinities and specificities. The findings should be helpful in advancing our understanding of the mechanisms whereby disordered amino acid sequences bind targets, modeling disordered proteins/regions, and computational prediction of binding affinities.