Cotton has sometimes been identified as the posthumous son of Anne Graves Cotton and William Cotton, the rector of Hungars Parish in Northampton County who died about 1640 or 1641, and as the John Cutten who with his wife Hannah Cutten, of that county, had a daughter in 1660 and a son in 1662, but extant records do not sustain either identification. The clergyman's only known surviving child was a daughter, and it has been impossible to establish any relationship between John Cotton and any members of the several Eastern Shore families whose surnames in the local records were spelled Cotten, Cotton, Cutten, Cutton, Cutting, or Cuttinge. The earliest known reference to John Cotton in Virginia documents is in the will of William Evans, of York County, which John Cotton and Ann Cotton witnessed on November 4, 1657, when a son of the Northampton clergyman would have been no more than sixteen years old. It is more likely that Cotton and his wife were married adults already living in York County by that date.

Nothing is known for certain about Cotton's origins, the date and place of his marriage or marriages, whether he had any children, or other details about his family; but his writings demonstrate that he received a good education and read widely in English and classical literature. York County records between 1657 and 1683 indicate that he lived on Queen's Creek, where for several years he owned a plantation. Although active as an agent and attorney, he did not serve on the county court, and there is no record of his holding a commission in the county militia.

Cotton was in Jamestown during the first week of June 1676 and saw the governor arrest and release Nathaniel Bacon, one of the episodes that set the rebellion in motion. Cotton's long narrative of the rebellion does not note whether he personally witnessed any of the other episodes he described, nor does it disclose what he himself did during that dramatic year. He appears to have had some sympathy with the rebels' initiative in defending the colony against the Indians, but he also sharply criticized Bacon for burning Jamestown. Cotton's name does not appear on any of the surviving documents that Bacon's supporters signed, nor on the official list of those who suffered property losses as a consequence of their adherence to the government of Sir William Berkeley.

The numerous similarities in wording, style, and content between a brief account of the rebellion that Ann Cotton wrote and the much longer one that has been attributed to John Cotton confirm his authorship, and her letter seems to substantiate that his was written first. His narrative was passed down through the Burwell family of Virginia and in 1814 was published for the first time as "The Burwell Papers" in the Collections of the Massachusetts Historical Society. Peter Force reprinted that version in the first volume of his Tracts and Other Papers, Relating Principally to the Origin, Settlement, and Progress of the Colonies in North America (1836). The 1814 edition being error-filled and modernized in spelling and punctuation, the Massachusetts Historical Society reprinted it in 1866 and at that time gave it the title by which it is usually known, "The History of Bacon's and Ingram's Rebellion." In 1915 Charles McLean Andrews reprinted the 1866 edition in his Narratives of the Insurrections, 1675–1690.

There is no sample of Cotton's handwriting by which to identify him as the person who indited the manuscript of his narrative that is at the Virginia Historical Society. That document appears to be in a late seventeenth- or early eighteenth-century handwriting, but the cover is dated July 27, 1764, in another hand. The text begins in mid-sentence on page five (the only numbered page) and ends abruptly in mid-sentence at the foot of the fifty-fifth page. The document is neither signed nor dated, and it contains no hint of the circumstances of the composition of the original. Another manuscript copy in the same library appears to be a transcription made for the printer's use in 1814 when the text was first published.

Cotton's narrative of the rebellion is witty, bombastic, and full of literary allusions, and as a consequence it is frequently quoted (almost always from the early and imperfect printed texts). Written in a florid style, it includes two poems, the first of which, "Bacon's Epitaph," has been lauded as the first notable poem composed in America, but it is not known whether Cotton wrote either or both of the poems. Cotton's original served as the basis for a much shorter account of the rebellion that his wife wrote and that was first published in 1804. That her account of the rebellion concludes with Berkeley's execution of the principal leaders suggests that his did, too, and that John Cotton may have composed his history not long after the execution, early in 1677. Cotton's original or another copy of it was probably the manuscript from which the Maryland poet Ebenezer Cooke derived his "History of Colonel Nathaniel Bacon's Rebellion in Virginia, Done into Hudibrastick Verse, from an Old MS," first published in The Maryland Muse in 1731.

There was more than one man named John Cotton in Virginia between the 1650s and 1680s, but only one is known for certain to have lived in York County. The last documented references to him in the records of that county concern a case that he evidently agreed on August 24, 1683, to postpone to the next meeting of the county court. At that meeting, on October 24, the justices of the peace postponed the case again. Cotton was presumably still alive on the latter date, but there is no further record of the case, and it may have abated as a consequence of his death a few days, weeks, or months later. His date of death and place of burial remain unknown.

Major Work

• "The History of Bacon's and Ingram's Rebellion" (ca. 1677; 1814, 1836, 1866, 1915)