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Uncovering key molecules that support parasite establishment is a prerequisite to interfere with this process. We identified Q586B2 as a <jats:italic>T. brucei<\/jats:italic> protein that induces IL-10 in myeloid cells, which promotes parasite infection invasiveness. Q586B2 is expressed during all <jats:italic>T. brucei<\/jats:italic> life stages and is conserved in all Trypanosomatidae. Deleting the Q586B2-encoding <jats:italic>Tb927.6.4140<\/jats:italic> gene in <jats:italic>T. brucei<\/jats:italic> results in a decreased peak parasitemia and prolonged survival, without affecting parasite fitness in vitro, yet promoting short stumpy differentiation in vivo. Accordingly, neutralization of Q586B2 with newly generated nanobodies could hamper myeloid-derived IL-10 production and reduce parasitemia. In addition, immunization with Q586B2 delays mortality upon a challenge with various trypanosomes, including <jats:italic>Trypanosoma cruzi<\/jats:italic>. 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