Because cells are machines, their structure determines their function (health). But their structure also determines cells’ mechanical properties. So if we can understand how cells’ mechanical properties are influenced by specific structures, then we can observe what’s happening inside of cells via mechanical measurements. The Atomic Force Microscope (AFM) has become a standard tool for investigating the mechanical properties of cells. In many experiments, an AFM is used to ‘poke’ adherent cells with nanonewton forces, and the resulting deformation observed via, e.g. Laser Scanning Confocal Microscopy. Results of such experiments are often interpreted in terms of continuum mechanical models which characterize the cell as a linear viscoelastic solid. This “top-down” approach of poking an intact cell —complete with cytoskeleton, organelles etc.— can be problematic when trying to measure the mechanical properties and response of a single cell component. Moreover, how are we to know the sensitivity of the cell’s mechanical properties to partial modification of a single component (e.g. reducing the degree of cross- linking in the actin cortex)? In contrast, the approach taken here —studying the deformation and relaxation of lipid bilayer vesicles— might be called a “bottom-up” approach to cell mechanics. Using Coarse- Grained Molecular Dynamics simulations, we study the deformation and relaxation of bilayer vesicles, when poked with constant force. The relaxation time, equilibrium area expansion, and surface tension of the vesicle membrane are studied over a range of applied forces. Interestingly, the relaxation time exhibits a strong force-dependence. Force-compression curves for our simulated vesicle show a strong similarity to recent experiments where giant unilamellar vesicles were compressed in a manner nearly identical to that of our simulations.