High intake of dietary salt (sodium chloride; NaCl) has been implicated in the development of hypertension, chronic inflammation and autoimmune diseases. We have recently shown that NaCl has a pro-inflammatory effect and boosts the activation of Th17 cells in vitro, with mice fed a high salt diet having an accelerated and more severe experimental autoimmune encephalomyelitis (Kleinewietfeld et al, Nature 2013). Here, we have examined how the activation of so-called alternatively activated or M2 macrophages is affected by NaCl. In stark contrast to our study with Th17 cells, we find that high salt decreased the activation of IL-4+IL-13 stimulated bone marrow-derived mouse macrophages (M(IL-4+IL-13)). Signature genes important for M2 activation, including Mrc1, Arg1, Ym1 and Fizz1, all had a blunted induction in the presence of NaCl; an effect which was not observed in tonicity controls (mannitol or urea), implying a specific action of NaCl. When co-cultured with naïve T cells stimulated with α-CD3+α-CD28, control M(IL-4+IL-13) macrophages suppressed T cell proliferation by 88%, whilst NaCl-blunted M(IL-4+IL-13) macrophages had a reduced suppression of 35%. Additionally, mice fed a high-salt diet had a reduced wound healing capacity; collectively indicating that salt perturbs M(IL-4+IL-13) function both in vitro and in vivo. To identify the mechanism by which salt mediates this effect, we performed genome-wide epigenetic modification (ChIP-seq for H3K4me3 and H4ac) analysis, together with assessment of transcriptional changes by microarray. The results of this revealed that NaCl modulated epigenetic marks at several genes important for M(IL-4+IL-13) activation. Additionally, gene ontology analysis indicated that M(IL-4+IL-13) macrophages with NaCl blunted activation had altered metabolism. Finally, Akt, a signalling pathway important for nutrient sensing and driving metabolism, was found to be reduced by salt, providing a novel mechanism by which NaCl perturbs M(IL-4+IL-13) activation and function. This study gives further support to the notion that the modulation of immune cell function by high dietary salt is relevant to hypertension and autoimmune diseases.