Variations in gene expression have been widely explored in order to obtain an accurate overview of the changes in regulatory networks that underlie phenotypic diversity. Numerous studies have characterized differences in genomic expression between large numbers of individuals of model organisms such as Saccharomyces cerevisiae. To more broadly survey the evolution of the transcriptomic landscape across species, we measured whole-genome expression in a large collection of another yeast species: Lachancea kluyveri (formerly Saccharomyces kluyveri), using RNAseq. Interestingly, this species diverged from the S. cerevisiae lineage prior to its ancestral whole genome duplication. Moreover, L. kluyveri harbors a chromosome-scale compositional heterogeneity due to a 1-Mb ancestral introgressed region as well as a large set of unique unannotated genes. In this context, our comparative transcriptomic analysis clearly showed a link between gene evolutionary history and expression behavior. Indeed, genes that have been recently acquired or under function relaxation tend to be less transcribed show a higher intraspecific variation (plasticity) and are less involved in network (connectivity). Moreover, utilizing this approach in L. kluyveri also highlighted specific regulatory network signatures in aerobic respiration, amino-acid biosynthesis and glycosylation, presumably due to its different lifestyle. Our data set sheds an important light on the evolution of intraspecific transcriptomic variation across distant species.