Polychaetes are vital for evaluating the effects of toxic metals in marine systems, and sensitive molecular biomarkers should be integral to monitoring efforts. However, the few polychaete markers that exist are inconsistent, even within the same species, failing to identify gene expression changes in metal-exposed animals incurring clear metabolic costs. Comparing previously characterised polychaete metal-responsive genes with those of another carefully selected species could identify biomarkers applicable across polychaetes. The ragworm Alitta virens (Sars, 1835) is particularly suited for such comparisons due to its dominance of fully saline coastal areas, widespread distribution, large biomass, and its phylogenetic position relative to other polychaete ‘omic’ resources. A transcriptome atlas for A. virens was generated and an RNASeq-qPCR screening approach was used to characterise the response to chronic exposures of environmentally relevant concentrations of copper and zinc in controlled mesocosms. Genes presenting dramatic expression changes in A. virens were compared with known metal-responsive genes in other polychaetes to identify new possible biomarkers and assess those currently used. This revealed some current markers should probably be abandoned (e.g. Atox1), while others, such as GST-Omega, should be used with caution, as different polychaete species appear to upregulate distinct GST-Omega orthologues. In addition, the comparisons give some indication of genes that are induced by metal exposure across phylogenetically divergent polychaetes, including a suite of haemoglobin subunits and linker chains that could play conserved roles in metal-stress response. Although such newly identified markers need further characterisation, they offer alternatives to current markers that are plainly insufficient.