The Erechtheion was begun in 421 BC, eight years after the death of Pericles in a plague that killed thousands of Athenians. While the Peloponnesian War did not conclude until 404 BC, a truce (the Peace of Nikias) permitted work to proceed as planned. The Erechtheion was a complex building intended to house the cults of local divinities and heroes that were intimately associated with the Acropolis. More importantly, it was a home to the ancient xoanon or wooden cult statue of Athena Polias.

Though there are no extant ancient references to the building's architect, it is likely to have been Mnesicles, who in 432 BC was forced to suspend work on the Propylaia, begun sixteen years earlier, in 437 BC. His authorship is borne out by the incorporation in both buildings of dark Eleusinian marble, the volumetric plasticity and the clever adaptation to changing levels in the site. Though work appears to have been briefly interrupted at one point, construction of the temple was completed in 405 BC. The following year Athens was forced to surrender to Sparta and accept defeat after almost three decades of fighting in the Peloponnesian war and endured the humiliation of a Spartan garrison encamped on the Acropolis. Nevertheless, for centuries after, the Erechtheion fulfilled its intended purpose as the sacred focus and culmination of the Panathenaic Festival.

The cults of at least ten deities and heroes were pulled together in this intricate building, which stood out on the north side of the Acropolis as a sculptural gem to be appreciated against the massive, simpler Parthenon. It is unlikely that the Erechtheion was given this name until much later. Originally, it would have been known as Temple of Athena Polias, having replaced a succession of earlier temples to this divinity. It may also have been called Archaeos Naos, in memory of its predecessor on the site, which was torn down by the Persians. Whatever the case, the principal deities to whom it was dedicated were Athena, Poseidon and (the deified) Erechtheus, first king of Athens, whose tomb was incorporated into the building. The tomb of the legendary Cecrops and the saltwater spring and trident marks said to have been created by Poseidon in the contest for patronage of Athens. The olive tree planted by Poseidon's rival Athena stood in the Pandroseion, a small walled precinct immediately to the west of the Erechtheion.