Background The mechanical properties that govern endothelial cell motion remain poorly understood, especially when these cells are part of a larger cellular community. To address this gap, we have developed a toolkit to quantify wide-ranging mechanical activities represented by cellular morphology, motion, and forces within individual cells and their neighboring region. Using this data, we generated Mechanomic Engagement Profile (MEP) maps that seek to define the functional identity of a cell type based on its degree of correlated engagement in multiple mechanical activities. Methods We cultured radially expanding more than 5 mm diameter colonies of endothelial cells from the pulmonary arteries (AEC), veins (VEC), and microvessels (MEC) of rat lungs. The substrate was 1.25 kPa, 100 µm thick, type-I collagen-coated polyacrylamide hydrogels. Building on the Monolayer Stress Microscopy technique and recent developments, we quantified various physical properties of advancing AEC, MEC and VEC monolayers1,2. MEP maps were generated using nonparametric Spearman covariance between mechanical activities. The data analysis was conducted using custom ImageJ and Python programs. Results MEP maps revealed systematic differences in the mechanical behavior of AECs, MECs and VECs. Consistent with MECs having tighter intercellular connections than AECs and VECs, the activities of individual MECs were better correlated with those in their neighboring region. Consistent with their relatively mature and stable intercellular junctions, the cells far from the migration front engaged more widely correlated activities than the cells near the migration front. Plithotaxis, a physical mechanism where local cellular motion is steered along local maximum principal stress orientation, was found to be enhanced not only with local maximum shear stress (as reported before) but also with strain energy in the substrate. Such enhancement of plithotaxis was strongest in MECs but absent in AECs, potentially suggesting MECs exhibit the most fluid-like behavior of the three cell lines3. Higher cytoskeletal tension was associated with faster motion in AECs and VECs but slower motion in MECs. In addition, stronger plithotaxis was associated with faster motion in AECs and MECs but unrelated to the motion of VECs. These observations indicate distinct mechanisms of migration in AECs, MECs and VECs. Conclusion By using the degree of correlation between various mechanical activities as an identity, the MEP maps provide a means to define the mechanistic fingerprint of AEC, MEC and VEC monolayers. MEP maps would help biologists design strategies for tissue engineering applications, examine functional consequences of molecular changes in the cells, or guide the search for a molecular source of a phenotypic change in the cells.