Urogenital chlamydial infections continue to increase with over 100 million people affected annually, causing significant economic and public health pressures. Whilst the role of traditional MHCI and II peptide presentation is well defined in chlamydial infections, the role of lipid antigens in immunity remains unclear. Natural Killer T (NKT) cells are important effector cells that recognise and respond to lipid antigen. Chlamydial infection of antigen-presenting cells facilitates presentation of lipid on the MHCI-like protein, CD1d, which stimulates NKT cells to respond. During urogenital chlamydial infection, CD1d-/- (NKT-deficient) female mice had significantly less chlamydial burden than WT mice, and also had significantly less incidence and severity of immunopathology in both primary and secondary infections. WT mice had significantly more reproductive tract lymphocytic infiltrate and 59% more fallopian tube occlusion (P<0.0016), and hence infertility, compared to CD1d-/- mice. Transcriptional array analysis of fallopian tubes day 6 post-infection revealed WT mice had elevated levels of IFNγ (6-fold), TNFα (38-fold), IL6 (2.5-fold), IL1β (3-fold), and IL17α (6-fold) mRNA compared to CD1d-/- mice. In infected females, both uterine and fallopian tissues had an elevated infiltration of CD4+ (but not CD8+) invariant NKT (iNKT) cells. Interestingly, infection of iNKT-/- (Jα18-/-) mice had no significant difference to WT mice on infertility suggesting that immunopathology is driven by a subset of semi-invariant NKT cells. Lipid mass spectrometry of infected macrophages expressing a cleavable CD1d protein revealed the chlamydial lipid profile presented to NKT cells. Taken together, these data reveal an immunopathogenic role on infertility for non-iNKT cells in chlamydial infections, facilitated by CD1d-restricted chlamydial lipid presentation by infected antigen-presenting cells.