Understanding the electrostatics of lipid membranes at a molecular level has the potential to offer great insight into the mechanism of voltage-gated processes but has been challenging to study experimentally. In this study, we characterize the equilibrium electric field fluctuations at the interfacial region of lipid bilayers by using a combination of ultrafast time-resolved infrared spectroscopy, molecular dynamics (MD) simulations, and spectral modeling. By monitoring the dynamics of the ester carbonyl stretching-vibration in hydrated phosphocholine lipid bilayers, we are able to measure a correlation function for the femtosecond and picosecond fluctuations in the local electric field of the membrane, estimating the standard deviation in these fluctuations as similar to 10MV/cm. The addition of gramicidin D at a 1:20 mol ratio with DMPC results in the formation of protein lipid hydrogen bonds, which alter the dynamics of the ester groups. Using MD simulations, we conclude that ultrafast local field fluctuations exist whether or not water interacts with the ester groups; however, water does accelerate the time-scale of these fluctuations.