Infectious laryngotracheitis (ILT) is an upper respiratory disease of chickens caused by a Gallid alpha herpesvirus-1 (GaHV-1), commonly known as infectious laryngotracheitis virus (ILTV). Vaccination remains necessary for the control of the disease. Earlier studies have pointed to the importance of the T cell-mediated immune responses for mediating vaccine protection. However, little is known about the T cell subtypes and the antiviral responses generated against ILTV. The objectives of these set of studies were to reveal the onset and differential T cell responses in the trachea during recall response to challenge in vaccinated chickens, and to assess the dynamic expression of interferons (IFNs) and interferon-stimulated genes (ISGs) in the trachea, larynx, and conjunctiva after vaccination or infection. Overall, the robust protection provided by the chicken embryo origin (CEO) vaccine was characterized by a minimal T cell infiltration into the tracheal mucosa after challenge. However, within this limited infiltration, the frequency of cytotoxic T lymphocytes (CTLs) and activated CTLs were increased early post-challenge. Partial protection induced by the tissue culture origin (TCO) and recombinant herpesvirus of turkey-laryngotracheitis (rHVT-LT) vaccines showed a significant infiltration of T cells into the tracheal mucosa. This was associated with an early but moderate increase in resting and activated CTLs, followed by enhanced NK cell responses after challenge. Non-vaccinated challenged chickens showed a significant infiltration of T cells and MRC1LB cells and a higher frequency of Tregs population than any of the vaccinates. After ocular inoculation, the CEO vaccine and virulent strains (63140 and 1874C5) induced sustained upregulation of ISGs expression either with or without limited upregulation of IFNs expression in the trachea and larynx. In contrast, TCO induced limited upregulation of IFNs and ISGs solely in the larynx. In the conjunctiva, the expression of type I IFNs was significantly downregulated after inoculation with CEO and virulent strains. Collectively, the studies described here comprehensively demonstrated that the T cells and the antiviral responses in the upper respiratory tract, and conjunctiva, are influenced differentially by the ILT vaccines, and that particular CTL recall response and ISGs induction by the CEO vaccine play a main role in vaccine protection.