The entire developmental history of muscle membrane electrogenesis can be observed in the embryonic myotubes of Drosophila. We have examined the development of ionic currents and muscle properties using whole-cell patch-clamp techniques throughout embryonic myogenesis. In the early stages of myogenesis, from myoblast fusion through to establishing epidermal insertions, the myotubes are electrically inert and are electrically and dye coupled to adjacent myotubes. Membrane electrogenesis begins in the mid-embryonic stages (early stage 16), when the myotubes abruptly uncouple, revealing the first of five prominent extrajunctional currents: a small, inward, voltage-gated calcium current (ICa). The uncoupling of the embryonic myotubes heralds the onset of extremely rapid electrogenesis; within several minutes both the fast, inactivating (IA; Shaker) and delayed, noninactivating (IK) outward potassium currents, the stretch-activated outward potassium current, and the junctional glutamate-gated inward current all appear and begin to develop in a current-specific manner. Very late in embryogenesis (late stage 17), the calcium-dependent, outward potassium currents [rapid, inactivating (ICF; slowpoke) then delayed, noninactivating (ICS)] develop, completing the complement of macroscopic currents in the mature larval muscle. Hence, the voltage-gated currents (ICa, IA, and IK, respectively) appear relatively early, and the calcium-dependent currents (ICF, ICS) appear only very late during myogenesis. This developmental progression of current maturation is reflected in dynamic changes in the voltage responses of the embryonic membrane, from wholly passive response to current injection in the early, coupled myotubes to regenerating, overshooting action potentials in the mature embryonic muscle. The earliest embryonic IA current has a midpoint of inactivation 40 mV more negative than the IA current in the mature embryo. As myogenesis proceeds, the inactivation curve develops a biphasic character, suggesting that a low-inactivation IA channel is present in early development and progressively replaced by the mature form as development proceeds. The current at all stages can be completely eliminated in Shaker mutants (ShKS133). These findings suggest that an embryonic form of the Shaker IA channel is present during early myogenesis. The prominent IA current present in early development is almost entirely inactivated at the physiological resting potential; the significance and mechanism of this developmental shift are unclear.