The church was founded on 9 September 1840.
 The service on that day was read by the first rector, Joseph Kidd Walpole, who had come to the district from Christ Church, Kelso, and had begun to plan the church building.
W. G. Broughton made an address at the ceremony.
 The anniversary sermon was preached by Robert Allwood.

This Foundation Stone of a church dedicated to the honor and worship of Almighty God!
and to be denominated 'The Church of St. John the Baptist' was laid the 9th day of September, 1840.
By the Right Reverend Father in God William Lord Bishop of Australia In the Fourth Year of the reign of Queen Victoria.
Sir George Gipps, Knight.
Governor.
Rev. Joseph Kidd Walpole, Minister.
Among those that are born of women there is not a greater Prophet than John the Baptist; but he that is last in the Kingdom of God is greater than he.
Luke vii, 28.

— Plaque inside the foundation stone, location unknown.

Building work on the church began in 1841, but construction came to a standstill due to construction problems and insufficient subscriptions.
The following year the colonial architect Edmund Blacket, as one of his first assignments after arriving in Sydney, was requested to inspect the church's walls, then still under construction.
 As a result of his report, the walls were demolished and re-erected, although continued funding problems, and the transfer of J. K. Walpole to Windsor caused further delays.
The church was licensed for operation on 1 October 1843.
Much of the interior woodwork was carved by the third rector, Frederick Wilkinson.
 The roof was strengthened in around 1845 by the installation of timber support columns.
 On 16 August 1845, at a cost of £100 the church purchased an additional 2.5 acres (1.0 ha) of land from Elizabeth Underwood (who remained a parishioner until her death, and is buried in a prominent grave within the church cemetery).
The church was eventually consecrated on 19 August 1845.

After 29 years, as the Bishop of Sydney Frederic Barker put it "the population of Sydney had invaded these sylvan shades", so an expansion was required.
Blacket designed the current stone transept and chancel, to transform the church into a cruciform plan.
 These were built during the period 1874–1875 at a cost of around £150 – raised without the help of grants from the government or the English societies.
The foundation stone of the addition was laid by Barker on 24 October 1874, and included a copy of Australian Churchman and the Sydney Morning Herald.
 At the time this addition accommodated an extra 250 seats, bringing the total capacity to 446.

Construction of the choir vestry and a wooden porch outside the western door were completed in 1885, and dedicated by Bishop Alfred Barry.
This work was overseen by the Blacket brothers,  who had followed the trade of their late father.

Arthur Blacket then designed the west tower.
The eight-bell peal was ordered from England after a generous bequest by one of the "Melanesian boys", David Marguay, and subsequent fundraising.
 The tower was then quickly constructed at a cost of around £250 in memory of the recently deceased rector James Christian Corlette, and dedicated as The Corlette Memorial Tower on 1 November 1901.
 The memorial bells proved depressing amongst the local populace, and were rearranged in 1904, with louvres added to the previously open arches.
 This was apparently ineffective, as the bells were removed within a few years.
The church was founded on 9 September 1840.  The service on that day was read by the first rector, Joseph Kidd Walpole, who had come to the district from Christ Church, Kelso, and had begun to plan the church building. W. G. Broughton made an address at the ceremony.  The anniversary sermon was preached by Robert Allwood.
This Foundation Stone of a church dedicated to the honor and worship of Almighty God! and to be denominated 'The Church of St. John the Baptist' was laid the 9th day of September, 1840. By the Right Reverend Father in God William Lord Bishop of Australia In the Fourth Year of the reign of Queen Victoria. Sir George Gipps, Knight. Governor. Rev. Joseph Kidd Walpole, Minister. Among those that are born of women there is not a greater Prophet than John the Baptist; but he that is last in the Kingdom of God is greater than he. Luke vii, 28.
— Plaque inside the foundation stone, location unknown.
Building work on the church began in 1841, but construction came to a standstill due to construction problems and insufficient subscriptions. The following year the colonial architect Edmund Blacket, as one of his first assignments after arriving in Sydney, was requested to inspect the church's walls, then still under construction.  As a result of his report, the walls were demolished and re-erected, although continued funding problems, and the transfer of J. K. Walpole to Windsor caused further delays. The church was licensed for operation on 1 October 1843. Much of the interior woodwork was carved by the third rector, Frederick Wilkinson.  The roof was strengthened in around 1845 by the installation of timber support columns.  On 16 August 1845, at a cost of £100 the church purchased an additional 2.5 acres (1.0 ha) of land from Elizabeth Underwood (who remained a parishioner until her death, and is buried in a prominent grave within the church cemetery). The church was eventually consecrated on 19 August 1845.
After 29 years, as the Bishop of Sydney Frederic Barker put it "the population of Sydney had invaded these sylvan shades", so an expansion was required. Blacket designed the current stone transept and chancel, to transform the church into a cruciform plan.  These were built during the period 1874–1875 at a cost of around £150 – raised without the help of grants from the government or the English societies. The foundation stone of the addition was laid by Barker on 24 October 1874, and included a copy of Australian Churchman and the Sydney Morning Herald.  At the time this addition accommodated an extra 250 seats, bringing the total capacity to 446.
Construction of the choir vestry and a wooden porch outside the western door were completed in 1885, and dedicated by Bishop Alfred Barry. This work was overseen by the Blacket brothers,  who had followed the trade of their late father.
Arthur Blacket then designed the west tower. The eight-bell peal was ordered from England after a generous bequest by one of the "Melanesian boys", David Marguay, and subsequent fundraising.  The tower was then quickly constructed at a cost of around £250 in memory of the recently deceased rector James Christian Corlette, and dedicated as The Corlette Memorial Tower on 1 November 1901.  The memorial bells proved depressing amongst the local populace, and were rearranged in 1904, with louvres added to the previously open arches.  This was apparently ineffective, as the bells were removed within a few years.
St John's, Ashfield