The physiological cellular partners that support T cell fate and long-term function remain to be systematically characterized. Here, using unbiased proximity labeling in combination with patient-based analyses, we systematically mapped the cellular interaction landscape of peripheral T cells. We identified monocytes as major cellular partners that physiologically form stable conjugates with activated T cells through the ICAM-1-LFA-1 adhesion axis. These interactions promote memory-associated T cell differentiation and support long-term T cell persistence. Mechanistically, monocyte-T cell conjugates facilitate the transfer of mitochondria and fatty acids from monocytes to T cells, promoting mitochondrial fatty acid oxidation, a metabolic feature associated with memory T cell states. Furthermore, monocyte-conditioned T cells exhibit improved persistence following adoptive transfer, highlighting a potential strategy to enhance the efficacy of T cell-based immunotherapies. Collectively, our findings identify monocytes as supportive cellular partners that sustain long-term T cell fitness through intercellular metabolic support.