CD4⁺ T helper 2 (T_H2) cells secrete interleukin (IL)4, IL5 and IL13, and are required for immunity to gastrointestinal helminth infections. However, T_H2 cells also promote chronic inflammation associated with asthma and allergic disorders. The non-haematopoietic-cell-derived cytokines thymic stromal lymphopoietin, IL33 and IL25 (also known as IL17E) have been implicated in inducing T_H2 cell-dependent inflammation at mucosal sites^,,,, but how these cytokines influence innate immune responses remains poorly defined. Here we show that IL25, a member of the IL17 cytokine family, promotes the accumulation of a lineage-negative (Lin^-) multipotent progenitor (MPP) cell population in the gut-associated lymphoid tissue that promotes T_H2 cytokine responses. The IL25-elicited cell population, termed MPP^type2 cells, was defined by the expression of Sca-1 (also known as Ly6a) and intermediate expression of c-Kit (c-Kit^int), and exhibited multipotent capacity, giving rise to cells of monocyte/macrophage and granulocyte lineages both in vitro and in vivo. Progeny of MPP^type2 cells were competent antigen presenting cells, and adoptive transfer of MPP^type2 cells could promote T_H2 cytokine responses and confer protective immunity to helminth infection in normally susceptible Il25^-/- mice. The ability of IL25 to induce the emergence of an MPP^type2 cell population identifies a link between the IL17 cytokine family and extramedullary haematopoiesis, and suggests a previously unrecognized innate immune pathway that promotes T_H2 cytokine responses at mucosal sites.