Key message Cucumber plants adapt their transcriptome and metabolome as result of spider mite infestation with opposite consequences for direct and indirect defences in two genotypes. Abstract Plants respond to arthropod attack with the rearrangement of their transcriptome which lead to subsequent phenotypic changes in the plants’ metabolome. Here, we analysed transcriptomic and metabolite responses of two cucumber ( Cucumis sativus ) genotypes to chelicerate spider mites ( Tetranychus urticae ) during the first 3 days of infestation. Genes associated with the metabolism of jasmonates, phenylpropanoids, terpenoids and l -phenylalanine were most strongly upregulated. Also, genes involved in the biosynthesis of precursors for indirect defence-related terpenoids were upregulated while those involved in the biosynthesis of direct defence-related cucurbitacin C were downregulated. Consistent with the observed transcriptional changes, terpenoid emission increased and cucurbitacin C content decreased during early spider-mite herbivory. To further study the regulatory network that underlies induced defence to spider mites, differentially expressed genes that encode transcription factors (TFs) were analysed. Correlation analysis of the expression of TF genes with metabolism-associated genes resulted in putative identification of regulators of herbivore-induced terpenoid, green-leaf volatiles and cucurbitacin biosynthesis. Our data provide a global image of the transcriptional changes in cucumber leaves in response to spider-mite herbivory and that of metabolites that are potentially involved in the regulation of induced direct and indirect defences against spider-mite herbivory. Electronic supplementary material The online version of this article (10.1007/s11103-020-01005-y) contains supplementary material, which is available to authorized users.