We have performed transcript and metabolite profiling of isolated cambial meristem cells of the model tree aspen during the course of their activity–dormancy cycle to better understand the environmental and hormonal regulation of this process in perennial plants. Considerable modulation of cambial transcriptome and metabolome occurs throughout the activity–dormancy cycle. However, in addition to transcription, post-transcriptional control is also an important regulatory mechanism as exemplified by the regulation of cell-cycle genes during the reactivation of cambial cell division in the spring. Genes related to cold hardiness display temporally distinct induction patterns in the autumn which could explain the step-wise development of cold hardiness. Factors other than low temperature regulate the induction of early cold hardiness-related genes whereas abscisic acid (ABA) could potentially regulate the induction of late cold hardiness-related genes in the autumn. Starch breakdown in the autumn appears to be regulated by the ‘short day’ signal and plays a key role in providing substrates for the production of energy, fatty acids and cryoprotectants. Catabolism of sucrose and fats provides energy during the early stages of reactivation in the spring, whereas the reducing equivalents are generated through activation of the pentose phosphate shunt. Modulation of gibberellin (GA) signaling and biosynthesis could play a key role in the regulation of cambial activity during the activity–dormancy cycle as suggested by the induction of PttRGA which encodes a negative regulator of growth in the autumn and that of a GA-20 oxidase, a key gibberellin biosynthesis gene during reactivation in spring. In summary, our data reveal the dynamics of transcriptional and metabolic networks and identify potential targets of environmental and hormonal signals in the regulation of the activity–dormancy cycle in cambial meristem.