Coccidiosis, a parasitic disease caused by Eimeria protozoa that parasitizes intestinal tissues of chicken, poses a challenge to the development of the poultry industry. circRNAs are a class of circular RNA macromolecules crucial in the immune response to pathogens. Previous studies have shown that gga-miR-2954 inhibits the inflammatory response to Eimeria tenella (E. tenella) infection. In this study, we screened the key circRNA (circNIPBLL) regulating gga-miR-2954 using a co-expression network. The RNase R and Actinomycin D assays showed that the circular structure of the circNIPBLL was stable. Besides, the circNIPBLL expression was mainly distributed in the cytoplasm but did not have coding capacity. Overexpression of circNIPBLL significantly promoted the production of the IL-6, IL-1β, TNF-α, and IL-8 in sporozoite-stimulated DF-1 cells, whereas circNIPBLL knockdown significantly inhibited these effects. Moreover, circNIPBLL induced apoptosis of DF-1 cells stimulated by sporozoites. Mechanistically, circNIPBLL functioned as a sponge for gga-miR-2954, and overexpression of circNIPBLL rescued the effect of gga-miR-2954 mimic on the inflammatory response of DF-1 cells stimulated with sporozoites. Taken together, this study suggested that circNIPBLL modulated the inflammatory response against E. tenella infection by sponging gga-miR-2954, which may provide novel insights into the immune mechanisms of chicken resistance to E. tenella.