Genome mergers between independently evolving lineages, via allopolyploidy, can potentially lead to instantaneous sympatric speciation. However, little is known about the consequences of allopolyploidy and the resultant “genome shock” on genome evolution and expression beyond the plant and fungal branches of the Tree of Life. The aim of this study was to compare substitution rates and gene expression patterns in two allopolyploid brown algae (Phaeophyceae, Heterokonta) and their progenitors in the genus Pelvetiopsis N.L. Gardner in the north-east Pacific, and to date their relationships. We used RNA-seq data and putative single-copy loci for phylogenomic, divergence and gene expression analyses. The multispecies coalescent placed the origin of allopolyploids in the late Pleistocene (0.35 – 0.05 Ma). Homoeologues displayed increased non-synonymous divergence compared with parental orthologues, consistent with relaxed selective constraint following allopolyploidization, including for genes with no evidence of pseudogenization or neo-functionalization. Patterns of homeologue-orthologue expression conservation and expression-level dominance were shared with both natural plant and fungal allopolyploids. Interestingly, gene expression also appeared partially linked to the gender of origin of homoeologues. Our results provide further support for common cross-Kingdom patterns of allopolyploid genome evolution and transcriptional responses, here in the evolutionarily distinct marine heterokont brown algae.