TREK‐1 (KCNK2) is a K_2P channel that is highly expressed in fetal neurons. This K⁺ channel is opened by a variety of stimuli, including membrane stretch and cellular lipids. Here, we show that the expression of TREK‐1 markedly alters the cytoskeletal network and induces the formation of actin‐ and ezrin‐rich membrane protrusions. The genetic inactivation of TREK‐1 significantly alters the growth cone morphology of cultured embryonic striatal neurons. Cytoskeleton remodelling is crucially dependent on the protein kinase A phosphorylation site S333 and the interactive proton sensor E306, but is independent of channel permeation. Conversely, the actin cytoskeleton tonically represses TREK‐1 mechano‐sensitivity. Thus, the dialogue between TREK‐1 and the actin cytoskeleton might influence both synaptogenesis and neuronal electrogenesis.