The hypothesis that all the vertebrates, including humans, share two ancestral rounds of whole‐genome duplications (WGDs/2R) is correct or not has recently become quite controversial. Furthermore, the contribution of hypothesised WGDs to the evolution of novel developmental features in modern vertebrates is still unclear. Attempts to settle these ardently debated issues have been hampered by small and noisy sequence data. Recently, based on advances in sequencing technology, hundreds of genomes spread across the whole metazoan tree have been decoded. This increasing amount of sequence data and recent advances in evo‐devo have set the stage for understanding metazoan evolution, including genomic innovations and accompanying developmental transitions. New sources of data provide insights into the vertebrate genome evolutionary history, notably the status of controversial 2R duplications. Key Concepts Duplication is considered to be an important source of new genes, hence providing a substrate on which evolution can work. Duplicated genes are often referred to as paralogous genes, which form multigene families. An understanding of the mechanisms of gene duplication is crucial for revealing how do newly duplicated acquire novel functions. All vertebrate animals including humans, despite their generally diploid state, carry large numbers of duplicated genes. Widespread existence of multigene families in vertebrates has been interpreted by some as evidence that two rounds of whole‐genome duplication (2R hypothesis) occurred at the origin of the vertebrates. Whether or not 2R occurred and what role it played in later evolution of vertebrates has been a contentious concept among evolutionary developmental biologists. This article provides more insight into the phenomenon by applying the recent knowledge developed largely through ever‐increasing number of sequenced genomes of bilaterian animals.