Rapid migration of naïve T cells through lymph node (LN) parenchyma and non-lymphoid tissue (NLT) is critical for detection of antigens and effective immune responses. Here we use in vitro and in vivo imaging to dissect the mechanics of naïve T cell migration in LN and determine how chemokine receptor CCR7, integrin LFA-1 and cortical actin contribute to intranodal locomotion. We find that T cells undergo periodic shape oscillations, where elongated shapes coincide with forward translocation and increased actin flow, which is quantitatively tuned by the strength of chemokine signaling. LFA-1 does not control cytoskeletal dynamics but creates tangential friction between actin cortex and environment, without adhesively confining the cells to lymph node stroma. In contrast to naïve T cells, we found that memory T cells migrating through NLT, such as salivary glands, do not require chemokines for efficient F-actin treadmilling or integrin coupling. Rather, integrin-independent intrinsic cell shape changes are sufficient and necessary for T cell surveillance of epithelial and non-epithelial compartments. The unexpectedly distinct dependencies of naïve and memory T cells on chemokines and integrins for efficient immune surveillance probably reflect the homogeneous structure of lymphoid organs versus the highly divergent NLT structure in terms of physical and biochemical properties.