BACKGROUND Among the Aristotelian senses, the subcellular and molecular mechanisms involved in the sense of touch are the most poorly understood. RESULTS We demonstrate that specialized sensory neurons, the class II and class III multidendritic (md) neurons, are gentle touch sensors of Drosophila larvae. Genetic silencing of these cells significantly impairs gentle touch responses, optogenetic activation of these cells triggers behavioral touch-like responses, and optical recordings from these neurons show that they respond to force. The class III neurons possess highly dynamic dendritic protrusions rich in F-actin. Genetic manipulations that alter actin dynamics indicate that the actin-rich protrusions (termed sensory filopodia) on the class III neurons are required for behavioral sensitivity to gentle touch. Through a genome-wide RNAi screen of ion channels, we identified Ripped Pocket (rpk), No Mechanoreceptor Potential C (nompC), and NMDA Receptors 1 and 2 (Nmdars) as playing critical roles in both behavioral responses to touch and in the formation of the actin-rich sensory filopodia. Consistent with this requirement, reporters for rpk and nompC show expression in the class III neurons. A genetic null allele of rpk confirms its critical role in touch responses. CONCLUSIONS Output from class II and class III md neurons of the Drosophila larvae is necessary and sufficient for eliciting behavioral touch responses. These cells show physiological responses to force. Ion channels in several force-sensing gene families are required for behavioral sensitivity to touch and for the formation of the actin-rich sensory filopodia.