Lymph nodes undergo a dynamic increase in size to accommodate immune responses repeatedly throughout a human’s lifetime. Upon immune challenge, antigen-activated DCs migrate to sentinel lymph nodes. These mature DCs have upregulated expression of CLEC-2 which binds to its ligand podoplanin (PDPN) expressed on the fibroblastic reticular cells (FRCs) which form the lymph node architecture. This interaction inhibits actomyosin contractility and causes relaxation of the FRC network which is necessary to accommodate the clonal expansion of lymphocytes during the acute phase of lymph node expansion. Mesenchymal cells including FRCs abundantly express the platelet derived growth factor-alpha (PDGFRα). We developed an inducible, knock-in mouse model to track and genetically manipulate FRCs (PDGFRα-mGFP-CreERT2), and used this to delete PDPN in FRCs. Lymph nodes were studied over a timecourse of several weeks after immunisation with IFA/OVA. We utilised flow cytometry to define the cell state of FRCs and impact of PDPN deletion on immune responses. Using confocal microscopy we studied changes to the tissue architecture, FRC network and in the balance of stromal cells to lymphocytes. We find that PDPN expression on FRCs is essential for maintaining tissue integrity and architecture in both steady state and for tissue remodelling through immune responses. In steady state, confocal microscopy revealed disruption in the compartmentalisation of T and B cells and the disruption of the FRC network. When mice were immunised following PDPN deletion the lymph nodes were unresponsive to the immune challenge. Using the PDGFRα-mGFP-CreERT2 x PDPN^fl/fl model we were able to identify the importance of PDPN beyond the inhibition of actomyosin contractility in FRCs during the acute phase of lymph node expansion. PDPN expression on FRCs maintains stromal cell interactions, lymph node compartmentalisation and drives immune responses in the lymph nodes.