Microscale mechanical properties of the extracellular matrix (ECM) and dynamic cell-ECM interactions play an important role in pathophysiological processes, including the onset, progression, and attenuation of disease. The ability to quantitatively image cell-mediated micromechanical dynamics of the ECM in physiologically relevant 3D engineered cellular systems can significantly enhance the clinical translational potential of fundamental discoveries in the rapidly growing field of mechanobiology. However, it remains a challenge for current mechanical characterization methods to combine quantitative 3D imaging of ECM mechanics with cellular-scale resolution and dynamic monitoring of cell‑mediated changes to pericellular viscoelasticity. Here, we present light-sheet photonic force optical coherence elastography (LS-pfOCE) to address this challenge by leveraging a light-sheet for parallelized, non-invasive, and localized mechanical loading. We demonstrate the capabilities of LS-pfOCE by imaging the micromechanical heterogeneity of fibrous 3D collagen matrices and perform a live-cell study to image micromechanical heterogeneity induced by NIH-3T3 cells seeded in 3D fibrin constructs. We also show that LS-pfOCE is able to quantify temporal variations in pericellular viscoelasticity in response to drug-induced altered cellular activity. By providing access to 4D spatiotemporal variations in the micromechanical properties of 3D biopolymer constructs and engineered cellular systems, LS‑pfOCE has the potential to drive new discoveries in mechanobiology and contribute to the development of novel biomechanics-based clinical diagnostics and therapies.