<p>Despite widespread immunization, <i>Bordetella pertussis</i> (<i>B. pertussis</i>) cases are resurging worldwide, prompting renewed interest in understanding the key mechanisms that underlie protective immunity. Similar to natural infection, immunization with whole-cell pertussis vaccines (wPV) generates long-lasting T_H1/T_H17 CD4 + T-cell responses that protect against <i>B. pertussis</i> infection. Additionally, wPV immunization generates robust tissue-resident memory T-cell responses (T_RM) that limit both pertussis disease and transmission. In contrast, acellular pertussis vaccines (aPV) generate short-lived T_H2-polarized immune responses that confer protection against severe disease but do not prevent <i>B. pertussis</i> colonization or transmission. Furthermore, the circulation of clinical strains with varied expression of aPV antigens also highlights the need for next-generation pertussis vaccines. Thus, coordinated innate and adaptive immune responses at the site of infection are required to effectively protect against <i>B. pertussis</i> colonization and persistence. This review integrates our current knowledge of natural and vaccine mediated T-cell immunity from both animal models and human studies to guide the development of improved pertussis vaccines capable of combating the resurgence of pertussis.</p>