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Infection of primary microglial cultures and murine cell lines with <jats:italic>Listeria<\/jats:italic> resulted in a dual function of the two gene expression programmes involved in early and late immune responses in macrophages. Whereas the bacterial gene <jats:italic>hly<\/jats:italic> seems responsible for both transcriptional programmes in macrophages, <jats:italic>Listeria<\/jats:italic> induces in microglia only the tumor necrosis factor (TNF)\u2010regulated transcriptional programme. <jats:italic>Listeria<\/jats:italic> also represses in microglia the late immune response gathered in two clusters, microbial degradation, and interferon (IFN)\u2010inducible genes. The bacterial gene <jats:italic>actA<\/jats:italic> was required in microglia to induce TNF\u2010regulated responses and to repress the late response. Isolation of microglial phagosomes revealed a phagosomal environment unable to destroy <jats:italic>Listeria<\/jats:italic>. Microglial phagosomes were also defective in several signaling and trafficking components reported as relevant for <jats:italic>Listeria<\/jats:italic> innate immune responses. This transcriptional strategy in microglia induced high levels of TNF\u2010\u03b1 and monocyte chemotactic protein\u20101 and low production of other neurotoxic compounds such as nitric oxide, hydrogen peroxide, and Type I IFNs. These cytokines and toxic microglial products are also released by primary microglia, and this cytokine and chemokine cocktail display a low potential to trigger neuronal apoptosis. This overall bacterial strategy strongly suggests that microglia limit <jats:italic>Listeria<\/jats:italic> inflammation pattern exclusively through TNF\u2010mediated responses to preserve brain integrity. 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