Urogenital Chlamydia trachomatis infects over 100 million people per annum and can cause inflammation, scarring, pelvic inflammatory disease and infertility in women. However, infections are often asymptomatic with an unknown underlying trigger for immunopathology. Male IgG serostatus to C. trachomatis is also a correlate of the disease outcome of female partners in fertility clinics. To determine the role of IgG during chlamydial infection we used IgG purified from infected male mice, incubated with C. muridarum and infected uterine epithelia in vitro, or the vagina of female mice. Opsonisation of Chlamydia enhanced infection of polarized uterine epithelial cells in vitro, but also transcytosed to the basolateral chamber, dependent on pH, concentration of IgG, and expression of the neonatal Fc receptor (FcRn). Female mice vaginally inoculated with opsonised Chlamydia had replicating Chlamydia in uterine sub-epithelia, but also in antigen present cells in the draining lymph nodes one day post inoculation, dependent of FcRn. In vitro infection of bone marrow-derived dendritic cells (CD11b+CD11c+) with opsonised Chlamydia significantly upregulated IL-1β, IFNγ, TNFα mRNA. In females mice there was no differences in chlamydial shedding over 35 days, but fallopian tube blockage was enhanced if mice were inoculated with opsonised Chlamydia. Opsonisation during inoculation led to the production of more Chlamydia-specific CD4+ and CD8+ T cells which secreted TNFα and IFNγ after 35 days. As CD8+ T cells are implicated in immunopathology, we also depleted mice of CD8β+ T cells on day two post-inoculation. In the absence of CD8+ T cells, pathology was equivocal to unopsonised controls. Taken together, these data demonstrate that male IgG seroconversion to chlamydial infection allows opsonisation of Chlamydia prior to sexual transfer, which can hijack and exacerbate inflammatory responses in females, dependent on FcRn, enhanced dendritic cell responses, and overproduction of immunopathogenic CD8+ T cells in the female reproductive tract.