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Bacterial pathogens sense specific cues associated with different host niches and integrate these signals to appropriately adjust the global gene expression. <i>Bordetella pertussis</i> is a Gram-negative, strictly human pathogen of the respiratory tract and the etiological agent of whooping cough (pertussis). Though <i>B. pertussis</i> does not cause invasive infections, previous results indicated that this reemerging pathogen responds to blood exposure. Here, omics RNA-seq and LC–MS/MS techniques were applied to determine the blood-responsive regulon of <i>B. pertussis</i>. These analyses revealed that direct contact with blood rewired global gene expression profiles in <i>B. pertussis</i> as the expression of almost 20% of all genes was significantly modulated. However, upon loss of contact with blood, the majority of blood-specific effects vanished, with the exception of several genes encoding the T3SS-secreted substrates. For the first time, the T3SS regulator BtrA was identified in culture supernatants of <i>B. pertussis</i>. Furthermore, proteomic analysis identified BP2259 protein as a novel secreted T3SS substrate, which is required for T3SS functionality. Collectively, presented data indicate that contact with blood represents an important cue for <i>B. pertussis</i> cells.