The controversy had been building since the reign of the Emperor Heraclius in the early seventh century. Heraclius had recovered large swaths of the empire from the Persians, but Syria and Egypt were full of Monophysites — Christians who believed Christ had only one nature, divine — and reconciling them with Constantinople's orthodoxy was a political as much as a theological problem. His solution was a doctrine called Monothelitism: Christ had two natures but one will. It was a compromise position, and like many compromises it satisfied no one completely. Jerusalem rejected it. Rome rejected it. Pope Martin I and the monk Maximus the Confessor held a synod in Rome in 649 condemning it outright. The Emperor Constans II, Heraclius's grandson, responded by arresting Pope Martin on charges of treason, sending him into exile, where he died. Maximus the Confessor was later tortured and mutilated. The theological dispute had, by now, consumed real lives.

It was Constantine IV who finally called the council, and the timing was significant. He had just successfully defended Constantinople against a Muslim siege that had lasted from 674 to 678 — the Umayyad fleet broken, the city relieved. With the external threat receded, internal unity with Rome became possible again. Constantine wrote to the Pope proposing a conference, and after some delays — the Pope he first wrote to had died before the letter arrived — the council was arranged. On 7 November 680, thirty-seven bishops and several priests gathered in a domed hall called the Trullus inside the Great Palace of Constantinople. The Emperor himself attended and presided over the first eleven sessions. The patriarchates of Alexandria and Jerusalem, both under Muslim rule, were represented not by their own patriarchs but by Byzantine appointees — a sign of how drastically the world had changed since the last great council.

The council's proceedings included, by any measure, one of the stranger moments in the history of Christian theology. A Monothelite priest named Polychronius, apparently convinced that God would validate his position through a miracle, claimed he could raise the dead. This was his proof: that his faith was correct, that Christ had only one will, and that the council should believe him. He had a corpse brought forward into the assembly. He knelt and whispered prayers into the dead man's ears. The body did not move. Undeterred by this outcome, Polychronius continued to profess Monothelitism and was formally anathematized by the council — condemned and excluded from the church. The incident is preserved in the records without editorial comment, which somehow makes it more vivid than any amount of theological argument.

The council concluded on 16 September 681, attended by 174 bishops by the final session. Its definition was clear: Christ has two wills and two energies, divine and human, and his human will is not contrary to but subordinate to his divine will. Monothelitism and Monoenergism were condemned as heresies. The Patriarch Macarius of Antioch, who had defended Monothelitism during the proceedings, was deposed. More controversially, the council retroactively condemned Pope Honorius I, who had died nearly fifty years earlier, for failing to clearly oppose the heresy during his pontificate — a condemnation that would resurface in the nineteenth century during debates over papal infallibility, since it showed that a council could judge a pope's doctrine deficient. The Third Council of Constantinople counts as the Sixth Ecumenical Council, recognized by both Eastern Orthodox and Catholic churches.

What the council reveals, more than any single theological conclusion, is Constantinople's extraordinary position in the seventh century. The city was under siege from the Arabs. Syria and Egypt had already been lost. The Persians had been pushed back but at enormous cost. And yet bishops still traveled here from the western edges of Christendom — from Milan, from Canterbury, from Rome — to argue about the nature of Christ's will in a domed hall inside the imperial palace. The council's location was not incidental: Constantinople was where these things got decided, where the universal church still had an addressable center, where the emperor and the patriarch and the bishop of Rome could, with effort, speak to each other. The city that housed this argument was also the city that would house its legacy — for another eight centuries, until 1453.