Memory T cells are heterogeneous in expression of lymph node homing receptors, delineating "central-memory" (T CM , CD62L hi /CCR7 + ) and "effector-memory" (T EM , CD62L lo /CCR7 -) subsets that migrate to lymphoid and non-lymphoid tissues, respectively. It is not known how these subsets arise or how homing receptor expression and tissue origin determine their functional and migratory properties. Here, we investigated the role of CD62L expression in the generation, function, distribution and migration of heterogeneous memory CD4 T cells specific for influenza hemagglutinin (HA). We found that CD62L hi and CD62L lo memory subsets are generated independent of CD62L expression by the activated precursor, and both subsets distribute into spleen and lung. Functionally, spleen-and lung-derived CD62L memory subsets produce effector cytokines at similar kinetics but differ strikingly in cell surface phenotype and migration: the CD62L lo memory subset expresses a classic memory phenotype (CD45RB lo /CD44 hi /CD11a hi ), while the CD62L hi subset expresses an unconventional phenotype (CD45RB hi /CD44 int /CD11a int ), defining a new polyclonal memory subset. The CD62L hi subset also trafficked more efficiently than CD62L lo cells into lymph nodes; however, only lung but not spleen CD62L lo memory T cells homed to lung. Our results reveal novel phenotypic heterogeneity of memory CD4 T cells co-segregating with CD62L expression and tissue-specific tropism of non-lymphoid memory CD4 T cells.