Developing quantitative models of intermolecular interactions within membrane components is crucial for establishing a general set of mechanistic principles that govern the coupling between environments and protein functions. Key questions that need to be addressed include the balance of forces stabilizing local lipidic environments around transmembrane proteins, the role of lipid-protein interactions in determining protein structure and stability, and the direct implications for protein function regulation. Formulating hypotheses remains challenging due to insufficient molecular information and the complexity of lipid-protein interactions. To advance beyond oversimplified membrane models requires new experimental approaches. Time-resolved and high-sensitivity vibrational spectroscopic methods discussed in this review show potential for providing molecular-level insights into these issues, revealing critical details about the structural and dynamic aspects of the interactions. In particular, the combination of time-resolved vibrational spectroscopy and molecular dynamics simulations is perfectly suited for investigating structure and dynamics at the interface over a range of timescales from picoseconds to milliseconds. These new approaches can help arrive at a comprehensive, molecular-level understanding of the interface, uncovering the impacts of interplay between lipid environments and proteins on associated functionality and biological processes. In the remainder of this review, we summarize the recent developments in ultrafast spectroscopies of model membranes, discuss the strengths and weaknesses of each approach, and provide some specific examples from recent research.