The traditional view of evolutionary mechanism holds that novel functions result from the modification of ancestral functions by natural selection. De novo gene origination was considered to be almost impossible until recent studies revealed that genes may arise from ancestrally non-genic sequence. Though such genes have been observed in several species, the dynamics of their origin and subsequent spread within populations remain completely obscure. Here I present results on the abundance, properties, expression genetics, and population dynamics of segregating and fixed de novo gene in Drosophila melanogaster populations from multiple tissues and developmental stages. These genes appear to derive primarily from ancestral intergenic, unexpressed sequences. Natural selection appears to play a significant role in the spread of these genes. These results reveal a heretofore unappreciated dynamism of gene content.