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Background  ETCHbox genes are eutherian-specific homeobox genes expressed during preimplantation development at a time when the first cell lineage decisions are being made. The mouse has an unusual repertoire of ETCHbox genes with several gene families lost in evolution and the remaining two,  Crxos  and  Obox , greatly divergent in sequence and number. Each has undergone duplication to give a double homeodomain  Crxos  locus and a large cluster of over 60  Obox  loci. The gene content differences between species raise important questions about how evolution can tolerate loss of genes implicated in key developmental events.    Results  We find that  Crxos  internal duplication occurred in the mouse lineage, while  Obox  duplication was stepwise, generating subgroups with distinct sequence and expression. Ectopic expression of three  Obox  genes and a  Crxos  transcript in primary mouse embryonic cells followed by transcriptome sequencing allowed investigation into their functional roles. We find distinct transcriptomic influences for different  Obox  subgroups and  Crxos , including modulation of genes related to zygotic genome activation and preparation for blastocyst formation. Comparison with similar experiments performed using human homeobox genes reveals striking overlap between genes downstream of mouse  Crxos  and genes downstream of human  ARGFX .    Conclusions  Mouse  Crxos  and human  ARGFX  homeobox genes are paralogous rather than orthologous, yet they have evolved to regulate a common set of genes. This suggests there was compensation of function alongside gene loss through co-option of a different locus. Functional compensation by non-orthologous genes with dissimilar sequences is unusual but may indicate underlying distributed robustness. Compensation may be driven by the strong evolutionary pressure for successful early embryo development.    Electronic supplementary material  The online version of this article (10.1186/s13227-018-0091-4) contains supplementary material, which is available to authorized users.

Mouse Obox and Crxos modulate preimplantation transcriptional profiles revealing similarity between paralogous mouse and human homeobox genes