[4] According to local traditions and 19th-century accounts, several Native American graves and ceremonial pits may have been uncovered during construction along Canton Avenue in Milton.

These discoveries, which were reported in local newsletters and oral histories, are believed to have belonged to members of the Ponkapoag tribe, who historically inhabited the area.

Graves found during roadwork were said to have been oriented east to west, potentially reflecting cultural or religious practices of the tribe.

Nearby pits, possibly used for cooking or religious ceremonies, were also reported, and evidence of long-term use, such as fire-scorched rocks and charcoal, was observed.

[7] The Ponkapoag tribe largely resided in the surrounding areas, including Canton and Stoughton, though some members, such as Mingo and his descendants, are recorded as having lived in Milton well into the 18th century.

The area that became Milton began to be sparsely settled by English colonists in the late 1620s and early 1630s as a part of Dorchester, formally established as an organized settlement in 1640 by Puritans from England.

Richard Collicott, one of the first English settlers, built a trading post near the Neponset River, and negotiated the purchase of Milton from Sachem Cutshamekin.

John Eliot, an English missionary, published a Massachusett translation of the Bible in 1640, facilitating rapid conversion of indigenous inhabitants to convert to Christianity and assimilate to the ideologies and culture of the colonists.

Furthermore, in 1640, English settlers began shipbuilding at Gulliver's Creek, a tributary of the Neponset, using the innumerable quantity of Eastern white pines found in early Milton's dense forests.

After incorporation, the population continued to increase during the late 17th century in the wake of King Philip’s War which had devastated much of New England.

The town was unscathed by the war due to several factors including the strategic location between hills, proximity to the well fortified capital Boston and most notably, the effective decimation of the indigenous inhabitants of the area by the 1660s as a result of disease and violent encroachment by colonists and the pacification of surviving Massachusett via mass conversions to Christianity and relocation to praying towns.

Boston investors, seeing the potential of the town and its proximity to the city, provided the capital to develop 18th-century Milton as an industrial area, including an iron slitting mill and sawmills, and the first chocolate factory in New England (the Walter Baker Chocolate Factory) in 1764, which was converted from the old Stoughton Grist Mill.

[11][12] The Suffolk Resolves, one of the earliest attempts at negotiations by the American colonists with the British Empire were signed in Milton in 1774, and were used as a model by the drafters of the Declaration of Independence in 1776.

Thomas Hutchinson maintained a summer estate called Unquity at the peak of Milton Hill, and during the increasingly violent revolutionary insurrections in Boston, he fled to Milton after his townhouse in the North End was burned by a mob and he was driven from the city after citizens learned he supported the suppression of Massachusetts by the British following the Boston Tea Party.

Both the neighboring house in which Hutchinson lived during the construction of his mansion and the barn of the estate still stand and are both privately owned.

Following the revolution, Milton continued to be a thriving agricultural and industrial town, greatly influenced both socially and economically by the prosperity of Boston and the newly-forged American identity.

As a result, much of Boston's elite built opulent country estates set on vast grounds throughout the idyllic hills and meadows of the town's more rural sections.

Like many other coastal American cities, high society would leave the cities for the summer, and in the case of Boston, many would move to Milton due to its rural qualities, proximity to Boston, its highly active mercantile wharf, and the families' factories in Lower Mills which allowed the tycoons to continue business in the summer months.

It is often called the first commercial railroad in the United States, as it was the first chartered railway to evolve into a common carrier without an intervening closure.

A centennial historic plaque from 1926 and an original switch frog and section of track from the railway can be found in the gardens on top of the Southeast Expressway (Interstate 93) as it passes under East Milton Square.

His company later sold the original hardtack crackers used by troops during the American Civil War due to their low potential for spoil.

The company, Bent's Cookie Factory, is still located in Milton and continues to sell these items to Civil War reenactors and others.

He built a Greek Revival mansion in 1833 at 215 Adams Street on Milton Hill, adjacent to the former site of Thomas Hutchinson's estate.

As a prominent example of Greek Revival architecture and possessing many artifacts from the China Trade period, the Captain Robert Bennet Forbes House is now listed on the National Register of Historic Places and is open for tours.

[16] The restrictive regulations sought to prohibit the kind of housing affordable to immigrants and minorities, which would serve to keep undesirable groups out of the town.

[16] During the mid to late 20th century, the character of the town changed from that of agriculture, industry, and rural retreat for the wealthy to suburban.

It is also often cited as being the windiest city in the United States, with an annual average wind speed of 15.4 mph (24.8 km/h) measured at the Blue Hill Meteorological Observatory.

[16] The town was sued by Massachusetts Attorney General Andrea Campbell after Milton voters voted in a February 2024 special election for the town to violate Massachusetts state law on housing and not comply with state law to permit multi-family housing near MBTA stations.