Significance We discovered that contrary to other bird species and most other animals, all examined songbird lineages contain a different number of chromosomes in the somatic and germline genomes. Their germ cells have an additional germline-restricted chromosome (GRC). GRCs contain highly duplicated genetic material represented by repetitive elements and sequences homologous to unique regions of the somatic genome. Surprisingly, GRCs even in very closely related species, vary drastically in size and show little homology. We hypothesize that the GRC was formed as an additional parasitic microchromosome in the songbird ancestor about 35 million years ago and subsequently underwent significant changes in size and genetic content, becoming an important component of the germline genome.