Chemokines and chemokine receptors rapidly diversified in teleost fish but their immune functions remain unclear. We report here that Chemokine (C-C motif) ligand 19 (CCL19), a chemokine known to control lymphocyte migration and compartmentalization of lymphoid tissues in mammals, diversified in salmonids leading to the presence of six CCL19-like genes named CK10a, CK10b, CK12a, CK12b, CK13a and CK13b. Salmonid CCL19-like genes all contain the DCCL conserved motif but share low amino acid sequence identity. CK12 (but not CK10 or CK13) is constitutively expressed at high levels in all four trout MALT. Nasal vaccination with a live attenuated virus results in sustained up-regulation of CK12 (but not CK10 or CK13) expression in trout NALT. Trout recombinant CK12a (rCK12a) is not chemotactic in vitro but it increases the width of the nasal lamina propria (LP) when delivered intranasally (I.N.). rCK12a delivered I.N or i.p. stimulates the expression of CD8α, granulysin, and IFNγ in mucosal and systemic compartments and increases nasal CD8α+ cell numbers. rCK12a is able to stimulate proliferation of head kidney leucocytes (HKLs) from antigen experienced trout but not naïve controls yet it does not confer protection against viral challenge. These results show that local nasal production of CK12a contributes to antiviral immune protection both locally and systemically via stimulation of CD8 cellular immune responses and highlights a conserved role for CK12 in the orchestration of mucosal and systemic immune responses against viral pathogens in vertebrates.