The dorsal part of the lateral geniculate nucleus (dLGN) is the main thalamic site for state‐dependent transmission of visual information. Non‐retinal inputs from the ascending arousal system and inhibition provided by γ‐aminobutyric acid (GABA)ergic local circuit interneurons (INs) control neuronal activity within the dLGN. In particular, acetylcholine (ACh) depolarizes thalamocortical relay (TC) neurons by inhibiting two‐pore domain potassium (K2P) channels. Conversely, ACh also hyperpolarizes INs via an as‐yet‐unknown mechanism. By using whole cell patch‐clamp recordings in brain slices and appropriate pharmacological tools we here report that stimulation of type 2 muscarinic ACh receptors (M2AChRs) induces IN hyperpolarization by recruiting the G beta‐gamma complex (Gβγ), class‐1A phosphatidylinositol‐4,5‐bisphosphate 3‐kinase (PI3K), and cellular and sarcoma (c‐Src) tyrosine kinase (TK), leading to activation of two‐pore domain weakly inwardly rectifying K+ channel (TWIK)‐related acid‐sensitive K+ (TASK)‐1 channels. The latter was confirmed by the use of TASK‐1 deficient mice. Furthermore inhibition of phospholipase Cβ (PLCβ) as well as an increase in the intracellular level of phosphatidylinositol‐3,4,5‐trisphosphate (PIP3) facilitated the muscarinic effect. Our results have uncovered a previously unknown role of c‐Src TK in regulating IN function in the brain and identified a novel mechanism by which TASK‐1 channels are activated in neurons. This article is protected by copyright. All rights reserved