Immunoglobulin E (IgE) plays an important role in allergic diseases. Nevertheless, the cellular and clonal origins of allergen-specific IgE, IgG1 and IgA secreting plasma cells (PCs) following allergen exposure are poorly understood. Here, we investigated their evolution and contribution to humoral immunity after house dust mite (HDM) allergen exposure using IgEVenus Blimp-1mCherry reporter mice. We show that short-term (< 4 weeks) allergen exposure results in the generation of IgE+ PCs that mainly reside in lung dLNs, while long-term exposure (>10 weeks) leads to the generation of long-lived IgE+ PCs that accumulate in the BM, maintain IgE serological memory and produce pathogenic IgE capable of inducing anaphylaxis. These IgE+ PCs first arise in dLNs (1-3 weeks post HDM exposure) and reach the BM after nine weeks of allergen challenge. Consistent with their accumulation in the BM, serum HDM-specific IgE levels significantly increase in mice at week 9. Moreover, unbiased computational data reduction and visualization highlight unique features of IgE+ PCs in the BM when compared to dLNs. Interestingly, when comparing IgM+, IgG1+, IgA+ and IgE+ PCs, each isotype clustered separately on UMAP plots, suggesting that PCs of different isotypes have distinct surface phenotypes. In addition, we show that IgE+ PCs are detectable in the lung at the same time as dLN (< 4 weeks). Overall, our findings highlight the unique developmental path and phenotypic signature of IgE PCs compared to other isotypes in allergic inflammation.