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Interleukin (IL) 21 is a pleiotropic cytokine that plays an important role in regulating innate and adaptive immune responses. In fish, the biological functions and cell source of IL-21 remain largely unknown. In this study, we performed qRT-PCR, Western blotting and immunofluorescent microscopy to examine the expression of IL-21 at the mRNA and protein levels. We found that <i>il21</i> expression was induced in the primary head kidney leukocytes of grass carp (<i>Ctenopharyngodon idella</i>) by heat-inactivated <i>Aeromonas hydrophila</i> (<i>A. hydrophila</i>) and LPS and in tissues after infection with <i>A. hydrophila</i>. Recombinant IL-21 protein produced in the CHO-S cells was effective in elevating the expression of antibacterial genes, including <i>β-defensin</i> and <i>lysozyme</i>, and, interestingly, inhibited the NF-κB signaling pathway. Furthermore, we investigated the response of the IL-21 expressing cells to <i>A. hydrophila</i> infection. Immunofluorescent assay showed that IL-21 protein was detected in the CD3γ/δ T cells and was markedly accumulated in the anterior, middle and posterior intestine. Collectively, the results indicate that IL-21 plays an important role in regulating the intestinal inflammation induced by bacterial infection in grass carp.