"This blessed place brings us back to our origins, to the births of our religions," the pope told those gathered Saturday in front of the 6,000-year-old ruins.
"Today we, Jews, Christians and Muslims, together with our brothers and sisters of other religions, honor our father Abraham," the pope said.
Once an important trading city of 60,000, the pope chose this archaeological site along the Euphrates River to share his message of reconciliation.
He thanked the Muslims communities' efforts to help rebuild Christian places of worship when Islamic State forces swept through the north of country in 2014. ISIS vowed to establish the headquarters of the caliphate in Iraq and bring their campaign to Rome. They even threatened to execute the pope.
"When terrorism invaded, it wantonly destroyed part of its magnificent religious heritage, he said. "I think of the young Muslim volunteers of Mosul, who helped to repair churches and monasteries, building fraternal friendships on the rubble of hatred, and those Christians and Muslims who today are restoring mosques and churches together."
Before arriving in Ur, Pope Francis paid a courtesy call to the Grand Ayatollah Sistani, a cleric revered by the Shia community.
Ayatollah Sistani, 90, is a reclusive figure who rarely receives international visitors. The visit was part of the Vatican's efforts to build a dialogue with the Shias and is an extension of St. John Paul II's policy of outreach to the other main religions.
Iraqi television carried live programming of the pontiff's arrival at to the ayatollah's home in the holy city of Najaf.
After the 45-minute meeting, the Vatican issued a statement saying the pontiff used the opportunity to thank the Shia cleric for speaking up "in defense of those most vulnerable and persecuted," and for affirming the "importance of the unity of the Iraqi people."
Demonstrating the importance of this expression of unity, Pope Francis continued onto Ur for a meeting of reconciliation where verses from the Quran and the Bible were recited. He also heard testimonies from Iraqis, including two friends of different religions who built a small business together.
"We don't want war and violence and hatred; we want that all people in our country work together and be friends," 19-year-old Dawood Ara, a Christian, told the pope.
Shias, Sunnis, Jews, Yazidis and even a member of the small Sabean Mandean community were invited to attend the event, though it is not clear if all were able to attend.
"Injustice has afflicted all Iraqis," Rafah Husein Baher, a Sabean Mandean told the pontiff. "Innocent blood was shed from all Iraqis."
But, she added, "Your visit is a triumph of virtue, much appreciated by Iraqis."
Pope Francis will visit the devastated Christian communities of the north of Iraq Sunday, where he will again use his visit to call for reconciliation.
"There will be no peace without sharing and acceptance," he told the Ur audience. "There will be no peace unless peoples extend a hand to other peoples. There will be no peace as long as we see others as them and not us."