Circadian clocks responsible for daily time keeping in a wide range of organisms synchronize to daily temperature cycles via pathways that remain poorly understood. To address this problem from the perspective of the molecular oscillator, we monitored temperature-dependent resetting of four of its core components in the fruitfly
Drosophila melanogaster
: the transcripts and proteins for the clock genes
period
(
per
) and
timeless
(
tim
). The molecular circadian cycle in adult heads exhibited parallel responses to temperature-mediated resetting at the levels of
per
transcript,
tim
transcript and TIM protein. Early phase adjustment specific to
per
transcript rhythms was explained by clock-independent temperature-driven transcription of
per
. The cold-induced expression of
Drosophila per
contrasts with the previously reported heat-induced regulation of mammalian
Period 2
. An altered and more readily re-entrainable temperature-synchronized circadian oscillator that featured temperature-driven
per
transcript rhythms and phase-shifted TIM and PER protein rhythms was found for flies of the ‘Tim 4’ genotype, which lacked daily
tim
transcript oscillations but maintained post-transcriptional temperature entrainment of
tim
expression. The accelerated molecular and behavioural temperature entrainment observed for Tim 4 flies indicates that clock-controlled
tim
expression constrains the rate of temperature cycle-mediated circadian resetting.