Genes and neural circuits coordinately regulate animal sleep. However, it remains elusive how these endogenous factors shape sleep upon environmental changes. Here, we demonstrate that Shaker (Sh)-expressing GABAergic neurons projecting onto dorsal fan-shaped body (dFSB) regulate temperature-adaptive sleep behaviors in Drosophila. Loss of Sh function suppressed sleep at low temperature whereas light and high temperature cooperatively gated Sh effects on sleep. Sh depletion in GABAergic neurons partially phenocopied Sh mutants. Furthermore, the ionotropic GABA receptor, Resistant to dieldrin (Rdl), in dFSB neurons acted downstream of Sh and antagonized its sleep-promoting effects. In fact, Rdl inhibited the intracellular cAMP signaling of constitutively active dopaminergic synapses onto dFSB at low temperature. High temperature silenced GABAergic synapses onto dFSB, thereby potentiating the wake-promoting dopamine transmission. We propose that temperature-dependent switching between these two synaptic transmission modalities may adaptively tune the neural property of dFSB neurons to temperature shifts and reorganize sleep architecture for animal fitness.