Loss of function mutations in human Caspase Recruitment Domain Containing Protein 9 (CARD9) cause invasive fungal infections, particularly of the central nervous system (CNS) with the fungus Candida albicans. CNS candidiasis is modeled in mice by intravenous injection to disseminate yeast cells throughout the body. However, at the challenge doses currently used, Card9-/- mice die from acute sepsis, making it difficult to relate findings to deep organ invasive candidiasis in humans with CARD9-deficiency. These human infections are often late-onset or chronic in nature and are not accompanied by acute sepsis. There is therefore an unmet need for the development of a model to study the pathogenesis of chronic tissue infections as well as the immune mechanisms underlying them. The recently identified p.Y91H mutation in CARD9 causes CNS candidiasis, however the immunological mechanisms by which p.Y91H leads to this disease remain to be fully characterized. We present a novel model of chronic invasive candidiasis in CARD9-deficiency with late onset chronology of disease symptoms. We show that p.Y91H knock-in mice (Y91HKI) phenocopy Card9-/- mice at the level of survival, dissemination, and tissue fungal burden but have divergent severity of neurological symptoms late in infection. Studies using the candidemia model of disseminated candidiasis have shown a granulopoietic response in the bone marrow and demonstrated that bone marrow hematopoietic stem and progenitor cells (HSPC) can proliferate in response to direct C. albicans challenge. We show that Card9-/- mice mount a robust, progressive, and transient emergency myelopoiesis response over the course of asymptomatic infection. Beta-glucan challenge in Card9-/- mice failed to induce HSPC expansion in vivo and Card9-/- BMDM from these mice showed augmented cytokine responses to C. albicans challenge in vitro. Together, our results show that Card9-/- mice mount a progressive emergency hematopoiesis response and suggest a role for CARD9 in fungal-induced trained immunity. By extending the chronology of disease, our work provides a new temporal framework for investigation of invasive candidiasis, and development of intervention strategies, by defining distinct phases of fungal growth, immune response, and disease in the context of CARD9 primary immunodeficiency.