St. John the Apostle, a Roman Catholic parish in Oregon City, was founded in 1844, more than a decade before Oregon attained statehood. One of the oldest Catholic parishes in the state, the church was the headquarters for the Diocese of Oregon City (now the Archdiocese of Portland) when the diocese was established in 1846.

Father Francis Blanchet and Dr. John McLoughlin traveled to Oregon City in 1843 to select a location for a new church and school near what is now 10th and Water Streets. Blanchet, one of the first priests to arrive in the Oregon Territory, was a missionary and vicar general of the Oregon Country. McLoughlin, chief factor of the Hudson's Bay Company and a devout Catholic, used his wealth to help both local Natives and resettlers who arrived in the region on the Oregon Trail. Baptized a Catholic but raised Anglican, McLoughlin had returned to the Catholic faith in 1842.

Father Modeste Demers, a missionary who had accompanied Father Blanchet to the Oregon Country from Quebec, was installed as the first pastor of St. John the Apostle on March 1, 1844, and celebrated the first Mass two days later. The cathedral at Oregon City—a wooden building in the shape of a cross, sixty feet long and thirty feet wide—was built in 1845 by pioneer carpenter Walter Pomeroy. The church's benediction was held on February 8, 1846.

By the time of the dedication, the Sisters of Notre Dame de Namur had arrived in St. Paul to open and manage a school for girls. In 1848, they were joined by seven sisters from Belgium, who ran a girls school in Oregon City until 1853, when the entire order moved to California. Sisters of the Holy Names opened a new parish school in 1860, which operated for two years before moving to Portland. And the Sisters of St. Benedict opened a parish school in 1885, which they ran for nearly a century. In 1907, Father Hillebrand created the McLoughlin Institute for elementary and secondary school children. It continues as St. John the Apostle Catholic School in a new hilltop location on 5th and Washington Streets.

The parish community grew up around the church, called the Cathedral of the Sacred Heart or the Sacred Heart Mission. In 1850, the Diocese of Oregon City was elevated to the Archdiocese of Oregon City. Archbishop Blanchet moved from Oregon City to Portland in 1862, and the cathedral church of the archdiocese became St. Mary’s Cathedral of the Immaculate Conception in Portland. The name of the archdiocese was officially changed to the Archdiocese of Portland in Oregon in 1928.

St. John the Apostle was the second Catholic parish dedicated in Oregon (the first was St. Paul), and the parish has remained significant in the history and culture of Oregon. John McLoughlin was not only involved in the beginnings of the parish, but he and his wife Marguerite were perhaps the most prominent parishioners and were instrumental in expanding Catholicism in the region, establishing the parish, funding missionary efforts, and setting an example for charity. In 1846, Pope Gregory XVI bestowed the Knighthood of St. Gregory the Great on McLoughlin for his work for the church. His and Marguerite's gravestones remained on parish property (at one time embedded in the expanded foundation) until 1970, when they were removed to the grounds of the McLoughlin House. 

The original chapel and other buildings that constituted St. John the Apostle parish were razed in 1947.  After World War II, new facilities were constructed at its present location on Washington Street. The building, along with a free-standing seventy-one foot tower with a fourteen-foot high gold anodited aluminum cross, was dedicated in 1957.