The current picture of embryonic development in nematodes is essentially shaped by Caenorhabditis elegans and its close relatives. As their pattern of embryogenesis is rather similar, it is often considered to be representative for the taxon Nematoda as a whole. Here we give for the first time a comprehensive description of embryonic development in an ancestrally diverged nematode. Romanomermis culicivorax differs strikingly from C. elegans with respect to cell division pattern, spatial arrangement of blastomeres and tissue formation. Our study reveals a number of unexpected phenomena. These include (i) unique polar interphase microtubule caps forming in early blastomeres destined to undergo asymmetric cleavages, suggesting the presence of a so far undescribed MTOC; (ii) embryonic cell lineages of reduced complexity with predominantly monoclonal sublineages, generating just a single tissue type; (iii) construction of major parts of the body from duplicating building blocks consisting of rings of cells, a pattern showing some resemblance to segmentation; (iv) prominent differences in cell fate assignment which can be best explained with a global shift affecting all somatic founder cells. In summary, our data indicate that during nematode evolution massive alterations in the developmental program took place of how to generate a juvenile.