Passive membrane permeation of small molecules is essential to achieve the required absorption, distribution, metabolism and excretion (ADME) profiles of drug candidates and is also central to transport across the blood-brain-barrier. Computational investigations of this process typically involve either building QSAR models, or performing free energy calculations of the permeation event. Although insightful, these methods rarely bridge the gap between computation and experiment in a quantitative manner, and identifying structural insights to apply towards the design of compounds with improved permeability can be difficult. In this work, we combine molecular dynamics simulations describing the kinetic steps of permeation at the atomistic level, with a dynamic mechanistic model describing permeation at the in vitro level, finding a high level of agreement with experimental permeation measurements. Calculation of the kinetic rates determining each step in the permeation event allows derivation of structure-kinetic relationships of permeation. We use these relationships to probe the structural determinants of membrane permeation, finding that the desolvation/loss of hydrogen bonding required to leave the membrane partitioned position controls membrane flip-flop rate, whereas membrane partitioning determines the rate of leaving the membrane.