The role of juvenile hormone (JH) in insect embryos is a mystery, especially in short germ-band hemimetabolan species. To shed light on this mystery, we depleted the mRNA levels of Kruppel homolog 1, Methoprene tolerant and JH acid O-methyltransferase, key elements of JH signaling, in embryos of the short germ-band hemimetabolan species Blattella germanica. This precluded the formation of the germ-band anlage in a group of embryos. Hatchability was also reduced, which may have been due to premature upregulation of laccase 2, a promoter of cuticle tanning. In other cases development was interrupted in mid embryogenesis, involving defects related to dorsal closure and appendages formation. These phenotypes are possibly due to the low levels of Broad-complex produced under JH-depleted conditions. This contrasts with holometabolan species, where JH does not promote BR-C expression, which remains low during embryo development. Possibly, the stimulatory role of JH on BR-C expression and the morphogenetic functions of BR-C in hemimetabolan embryos were lost in holometabolan species. If so, this may have been a key driver for the evolution of holometabolan metamorphosis.