Dynamic interactions between peptides and lipid membranes are crucial in many biological processes and biomedical applications. Monitoring peptide dynamics in a membrane environment has been limited by the lack of experimental methods that could directly detect the fast (picosecond to nanosecond) timescale dynamics of peptides in this environment. Spin relaxation times from NMR experiments are sensitive to such motions, but their applications are often limited by complications in sample preparation and interpretation of the data. Here we show that the detailed dynamic landscape of peptide-membrane mimics can be determined by a synergistic combination of solution state NMR experiments and molecular dynamics (MD) simulations. Solution state NMR experiments are straightforward to implement without an excessive amount of sample, while direct combination of spin relaxation data to MD simulations enables detailed interpretation of dynamic landscapes of both peptide and membrane mimics. The interpretation of NMR data from transmembrane, peripheral, and tail anchored peptides indicate that peptides and detergent molecules do not rotate together as a rigid body, but rotate in a viscous medium composed of detergent micelle. Spin relaxation times also provide indirect information on peptide conformational ensembles. This work gives new perspectives on peptide conformational ensembles and dynamics in membrane environments.