While plasmacytoid dendritic cells (pDCs) produce outstanding amounts of type I interferons (IFN-I), conventional (c) DCs specialize in antigen presentation. We previously demonstrated that following a viral infection, pDCs lose their capacity to produce IFN-I while converting into cDC-type-2 (cDC2s). However, these studies did not exclude recently described pDC-like DCs (also known as transitional DCs), which lack IFN-I production capacity and convert into cDC2s, underscoring the need to re-contextualize past results with pDC specific markers that are discriminative after infection. Here, leveraging CITE-seq, we mapped pDC transcriptional and protein landscapes following a viral infection and identified two canonical pDC subsets distinguished by differential CCR9 expression. Both subsets produced IFN-I upon stimulation when isolated from uninfected mice, but completely lost this function after infection. Ex-vivo and in-vivo experiments demonstrated that both pDC subsets converted into cDC2s after infection, being CCR9low pDCs more efficient and able to generate both CCR9high pDCs and pDC-like DCs, highlighting its exceptional plasticity. Importantly, pDC-subset–derived cDC2s activated and induced proliferation of virus-specific CD4 T cells comparably, outperforming cDC2s derived from pDC-like cells. Finally, we showed that pDC subset conversion into cDC2 took place without proliferation and was counteracted when recombinant IFN-a was added to the culture ex-vivo. Together, our findings identify two canonical pDC subsets present during in vivo viral infection and demonstrate that both subsets lose their capacity to produce IFN-I while enhancing their conversion into cDC2s with high T cell-stimulatory potential. We also show that the CCR9low pDCs display the greatest conversion capability highlighting its potential as a therapeutic target.