Athenians thought of themselves as Erechtheidai, the "sons of Erechtheus." In Homer's Iliad (2.547–48) Erechtheus is the son of "grain-giving Earth," reared by Athena. The earth-born son was sired by Hephaestus, whose semen Athena wiped from her thigh with a fillet of wool cast to earth, by which Gaia was made pregnant.

In the contest for patronage of Athens between Poseidon and Athena, the salt spring on the Acropolis where Poseidon's trident struck was known as the "sea of Erechtheus."

The second Erechtheus was given a historicizing genealogy as son and heir to King Pandion I of Athens by Zeuxippe, this Pandion being son of Erichthonius. This later king Erechtheus may be distinguished as Erechtheus II. His siblings were Philomela, Procne, Butes and possibly Teuthras.

Erechtheus was father, by his wife Praxithea, of the sons Cecrops, Pandorus and Metion, and of six daughters: Protogeneia (the eldest), Pandora, Procris, Creusa, Oreithyia and Chthonia. Among other children sometimes named are Orneus, Thespius, Eupalamus, Sicyon and Merope.

According to Pseudo-Apollodorus, Erechtheus II had a twin brother named Butes who married Erechtheus' daughter Chthonia, the "earth-born." The brothers divided the royal power held by Pandion, Erechtheus taking the physical rule while Butes took the priesthood of Athena and Poseidon, a right passed on to his descendants. This late origin myth, or aition, justified and validated the descent of the hereditary priesthood of the Boutidai family.

His reign was marked by the war between Athens and Eleusis, when the Eleusinians were commanded by Eumolpus, who came from Thrace. An oracle declared that Athens' survival depended on the death of one of the three daughters of Erechtheus — perhaps meaning the three unmarried daughters. In one version it is Chthonia, the youngest, whom he sacrifices; in another, it is both Protogeneia and Pandora, the two eldest, who offer themselves up. In any case the remaining sisters (excepting Orithyia, who had been kidnapped by Boreas), or at least some of them, are said to kill themselves. The story of the unfortunate daughters of Erechtheus is comparable to those of the daughters of Hyacinthus of Lacedaemon and of the daughters of Leos.

In the following battle between the forces of Athens and Eleusis, Erechtheus won and slew Eumolpus, but then himself fell, struck down by Poseidon's trident. According to fragments of Euripides' tragedy Erechtheus, Poseidon avenged the death of his son Eumolpus by driving Erechtheus into the earth with blows of his trident.

The closing lines of Euripides' tragedy were recovered in 1965 from a papyrus fragment. They demonstrate, for Burkert, that "the founding of the Erechtheum and the institution of the priestess of Athena coincide." Athena resolves the action by instructing Erechtheus' widow Praxithea to build a shrine for her husband in the middle of the city: he is to be known after the one who killed him, under the name "sacred Poseidon," but among the citizens, when sacrificial cattle are slaughtered, he shall also be called "Erechtheus." Praxithea, having rebuilt the city's foundations, is granted the duty of bringing the preliminary fire-sacrifices for the city and is to be called Athena's priestess.

In the Athenian king-list, Xuthus, the son-in-law of Erechtheus, was asked to choose a successor from among his many sons and chose Cecrops II, named for the mythic founder-king Cecrops. Thus, according to a fragment from the poet Castor, Erechtheus is succeeded by Cecrops II; but according to Pseudo-Apollodorus he was succeeded by his own son.

The central gods of the Acropolis of Athens were Poseidon Erechtheus and Athena Polias, "Athena patron-guardian of the city." The Odyssey (VII.81) already records that Athena returned to Athens and "entered the strong-built house of Erechtheus." The archaic joint temple, built upon the spot identified as the Kekropion — the hero-grave of the mythic founder-king Cecrops and the serpent that embodied his spirit — was destroyed by the Persians in 480 BC during the Greco-Persian Wars, and was replaced between 421 and 407 BC by the present Erechtheum. The site's continuity is reflected in Nonnus' Dionysiaca, which calls the Erechtheion lamp "the lamp of Cecrops." Priests of the Erechtheum and the priestess of Athena jointly took part in the procession to Skiron that inaugurated the Skira festival near the end of the Athenian year; their object was the temenos at Skiron of the hero-seer Skiros, who had aided Eumolpus in the war between Athens and Eleusis in which Erechtheus II was both triumphant and died.

That Poseidon and Erechtheus were two names at Athens for the same figure was demonstrated in the cult at the Erechtheum, where there was a single altar, a single priest, and sacrifices dedicated to Poseidon Erechtheus, as Walter Burkert observed. He added: "An historian would say that a Homeric, pan-Hellenic name has been superimposed on an autochthonous, non-Greek name."

Swinburne's classical tragedy Erechtheus was published in 1876. He uses the framework of the classical myth to express the republican and patriotic ideals that preoccupied him at this era.