On the north side of the agora once stood the Stoa Poikile, the Painted Stoa, built in the fifth century BC and unusual among the agora's buildings because it served no commercial or administrative purpose. People gathered there to argue. Zeno of Citium chose its colonnade as the place to teach his philosophy, which is why Stoicism still bears the name of this porch. To the south stood the Stoa of Attalos, lined with shops, given to Athens as a diplomatic gift by Attalos II of Pergamon in the second century BC. East of that stretched the Library of Pantainos, which was more than a library; its west and north wings rented rooms to marble-workers, lawyers, and other trades that needed a roof and an address near the agora's official entrance.

The west side of the agora carried the actual machinery of Athenian government. The Bouleuterion housed the Council of Five Hundred. The circular Tholos beside it served as dining hall and overnight quarters for the rotating prytaneis, the standing committee that ran the city day to day. The Metroon held the public archives and the cult of the Mother of the Gods. Outside these buildings stood the Monument of the Eponymous Heroes, ten bronze statues representing the ten tribes of Athens, with a public notice board running below them. New legislation went up here. Military conscription lists went up here. Public events were posted here. A free male citizen of Athens was expected to read the board on his way through the agora and act on what it said. Behind the monument rose the Temple of Hephaestus, the best-preserved Doric temple anywhere in Greece, still standing nearly complete on Agoraios Kolonos.

Athenian democracy excluded women from voting, but the agora was not a male-only space. In the fourth and fifth centuries BC, women ran inns and sold their own wares: fruit, clothes, pottery, religious goods, perfume, incense, purple dye, ribbons, and wreaths. Religious festivals on the Athenian calendar gave women of all classes a public role, and aristocratic daughters were required to officiate the worship of Athena. They built personal memorials to their piety inside the agora, paid for from their own funds. A 1974 excavation turned up a small lead tablet inscribed by an enslaved man named Lesis. The letter pleads with his mother to find someone to rescue him from the bronze workshop where he had been bound to labor. It is one of the very few surviving texts in any classical language written by an enslaved person. The agora was a place of citizenship and a place of bondage at the same time.

Before 1931, this whole area was a working Athenian neighborhood called Vrysaki, full of houses and small shops. The Greek state could not afford to expropriate it for excavation, so the American School of Classical Studies at Athens raised money from John D. Rockefeller Jr. and bought the land. Director T. Leslie Shear hired Greek photographer Messinesi to document the neighborhood before its demolition. Then the houses came down. Excavations began in 1931 under Shear, with Homer Thompson, Dorothy Burr, Virginia Grace, and others on the team; Shear's wife, Josephine Platner Shear, supervised the digging and the numismatics. By 1935, almost 600 sculptures, 6,000 pottery fragments, and 41,000 coins had emerged. The 1939 season removed 56,000 tons of earth in a single year. In the 1950s, Homer Thompson rebuilt the Stoa of Attalos as the museum and headquarters for the dig. Director John McK. Camp ran the project from 1994 until his retirement in 2022; John K. Papadopoulos directs the work today.