Low temperatures can be fatal to insects, but many species have evolved the ability to cold acclimate, thereby increasing their cold tolerance. It has been previously shown that Drosophila melanogaster larvae perform cold-evoked behaviors under the control of noxious cold-sensing neurons (nociceptors), but it is unknown how the nervous system might participate in cold tolerance. Herein, we describe cold-nociceptive behavior among 11 drosophilid species with differing cold tolerances. Behavioral analyses revealed that the predominant cold-evoked larval response is a head-to-tail contraction (CT) behavior, which is likely inherited from a common ancestor, but with characters not wholly consistent with the behavior being protective.  We therefore tested the hypothesis that cold nociception functions to protect larvae by triggering cold acclimation. Via a combination of neurogenetics and electrophysiology, we show that Drosophila melanogaster Class III nociceptors are sensitized by and critical to cold acclimation.  Moreover, we demonstrate that cold acclimation can be optogenetically-evoked, sans cold.  Collectively, these findings demonstrate that cold nociception constitutes a peripheral neural basis for Drosophila larval cold acclimation.