Prominent in the religious and political life of Melbourne's middle classes from the earliest days of European settlement, the Congregationalist Church counted John Pascoe Fawkner among its adherents. Its first minister, William Waterfield, arrived in Melbourne in 1838 under the patronage of merchant Henry Hopkins. His followers built Melbourne's first permanent place of worship between September 1839 and January 1841, on land in Collins Street East granted in 1838 by the NSW colonial government. The arrival of three ministers in 1849 allowed the creation of 13 new congregations in the colony by 1855. In 1852 the Congregational Union of Victoria was founded, but it collapsed in 1856 following intense controversy over the issue of state aid, and was not refounded until 1860. The denomination's civic profile expanded in 1866 with the appointment of the dynamic preacher Anketell Henderson as minister at Collins Street Independent Church, and the construction of a new building on the site. Designed by Reed & Barnes, the Romanesque church's distinctive tower remains a key feature of Melbourne's cityscape.
The independent polity of the Congregationalists allowed remarkable growth in some churches, but produced intense strife in others. By 1900 there were 12 Congregationalist churches within 2 miles (3 km) of the General Post Office, but few new congregations were established in the 20th century. The first female minister, Isabelle Merry, was ordained in 1937. While the insistence on freedom of belief attracted leading middle-class liberals, the church was comparatively under-represented in education. A theological college, founded in Carlton in 1862, merged with the Uniting Church Theological Hall when all but one Congregationalist church joined the Uniting Church of Australia in 1977.