As early as June 1594, 'Orchestra, or a Poeme of Dancing' by John Davies was entered in the Stationers' Registers, but the first extant edition is dated 1596. From the dedicatory sonnet to Richard Martin we learn that this graceful and brilliant poem was written in the space of fifteen days. In July 1595, Davies was called to the bar and, in February 1598, for a grave breach of discipline, he was disbarred. Richard Martin of the Middle Temple, a noted wit, to whom 'Orchestra' had been dedicated, appears to have provoked Davies by his raillery. While Martin was dining at the barristers' table, Davies entered the hall, attended by two persons armed with swords. Pulling a cudgel from under his gown, he broke it over Martin's head. He then fled in a boat from the Temple Steps on the Thames. Upon his expulsion from the Middle Temple, he returned to Oxford "in the condition of a sojourner"; and, during his retirement, composed, in quatrains, his terse and subtle poem on the immortality of the soul, 'Nosce Teipsum,' which was published in 1599 with a dedication to Queen Elizabeth I. In one manuscript copy there is a dedication to the Earl of Northumberland, who befriended Davies after his expulsion from the Middle Temple.

In Trinity term 1601, Davies petitioned to be restored to the Middle Temple and, in the following November, after making an open apology to Martin, he was readmitted to the society. In the same year, he was returned to Parliament for Corfe Castle in Dorset and he was one of the members of a parliamentary 'grand committee' appointed to thank the Queen for withdrawing certain obnoxious patents. When Sir Robert Cecil entertained the Queen, in 1602, at his new house in the Strand, Davies composed 'A Contention betwixt a Wife, a Widow and a Maid' for the occasion. On the death of Queen Elizabeth in March 1603, Davies accompanied her cousin, Lord Hunsdon, in his hasty journey to the Scottish Court. King James, on hearing that Davies was the author of 'Nosce Teipsum,' "embraced him and conceived a considerable liking for him". While Davies was in Scotland, his influence was solicited by Francis Bacon, who occasionally corresponded with him in later years.

On 18th September 1603, the King wrote to Lord Mountjoy, Lord-Lieutenant of Ireland, ordering a grant of the office of Solicitor-General for Ireland to be passed under the Great Seal to Davies. The following November, Davies arrived in Dublin to assume the office. A few days after his arrival, he sent to Cecil a graphic account of the state of Ireland. Pestilence and famine were raging and "the face of things appeared very miserable". But his first gloomy impressions were dissipated when he observed that the law courts were commanding respect. "I conceive," he writes, "a very good hope that after a parliament wherein many mischiefs maybe removed and prevented, and after the people are acquainted with the forms of justice ... this kingdom will grow humane and civil ..." On 20th February 1604, he sent to Cecil from Castle Reban - 'a remote and solitary place' - another long letter, in which he complained of the slothfulness and ignorance of the Protestant clergymen, whom he described as 'mere idols and ciphers, and such as cannot read their neck-verse if they should stand in need of the benefit of their clergy". He found churches ruined and preaching neglected and he prays that commissioners may be sent from England to inquire into these abuses. In the same letter, he complains of the facility with which the King's pardon could be obtained in cases of robbery and murder, points out the desirability of holding quarter sessions and condemns the base coinage. His third letter to Cecil is dated from Dublin, 7th March 1604. On 19th April 1604, he announced to Cecil that he had been on circuit over the greatest part of Leinster. Sessions had been held in seven shires and no difficulty had been found in securing competent jurors.

In April 1605, Davies proceeded to England with Sir Richard Cooke, Chief Baron, to report on the state of Ireland, taking with him a letter to the Lords of the Council, in which his "industrious pains" and "toilsome travels through most part of the kingdom" were highly commended by Sir Arthur Chichester, the Lord Deputy. He returned in July 1605. The Lords of the Council showed their appreciation of his services by urging Chichester to pay the arrears of his allowance.

One object towards which Davies diligently directed his efforts was the banishment of Roman Catholic priests from Ireland and the establishment of the Protestant religion. During his short visit to England, he seems to have thoroughly impressed his views on the English authorities for, upon his return to Ireland, strict measures were taken to expel the priests and enforce the attendance of people at church. On 23rd November 1605, he delivered a powerful speech in the Court of Castle Chamber when the recusants were summoned to answer their contempts against the King's proclamations. He tells Cecil, soon after, that if the one corporation of Dublin were reformed, the example would be quickly followed by the rest of the community. Believing that "the multitude was ever made conformable by edicts and proclamations," he beseeches Cecil not to despair of reducing the recusants to obedience. Another of Davies' letters to Cecil, dated 4th May 1606, gives a very valuable account of the state of Munster, where he had been holding the assizes.

On the elevation of Sir Charles Calthorpe to the bench, Davies succeeded to the post of Attorney-General for Ireland, on 29th May 1606, and he was afterwards called to the degree of sergeant-at-law. In the Summer vacation of that year, he made a journey through Monaghan, Fermanagh and Cavan, and recorded his 'observations' in a long letter to Cecil. In the Summer of 1607, he went on circuit through the counties of Meath, Westmeath, Longford, King's County and Queen's County, and reported to Cecil that it was almost a miracle to see the quiet and conformity which everywhere prevailed. A few weeks afterwards, in September 1607, he sent Cecil a full relation of the flight of Tyrone and Tyrconnell. In January 1608, he went to Ulster to indict the fugitive earls. He sent privately to Cecil a copy of the indictment, and announced that the proceedings for outlawing the earls would be completed at the beginning of Trinity term.

In July, the Lord Deputy, with Davies and other commissioners set out from Dublin to Ulster to view the escheated lands. A letter from Davies to Cecil, dated 5th August 1608, gives a picturesque account of the journey, describing how the "wild inhabitants" of the remoter districts "wondered as much to see the King's Deputy as the ghosts in Virgil wondered to see Aeneas alive in hell". A second commission for the plantation of Ulster was appointed in 1609, and a third in 1610. Davies, who showed great zeal in the work, was despatched in October 1608 to England with Sir James Ley, the Lord Chief Justice, in order to acquaint the Lords of the Council with the details of the proposed settlement. For his services in the matter of the plantation, the King conferred on him, by patent dated 29th May 1609, the dignity of a Serjeant, and directed that he should receive a grant of lands to the value of £40 per annum. About March 1609, he married Eleanor, daughter of George Touchet, Lord Audley (later Earl of Castlehaven). He returned to Ireland in June 1609 but, in February 1610, was again in London on business connected with the commission. During his stay in London, he addressed a letter to Cecil expressing a hope that he may be recalled as soon as the work of the commissioners is ended, for Irish affairs, he writes, "are in so improved a condition that any English lawyer would be competent to take his place". In July and August 1610, the commissioners set themselves to carry out the scheme of plantation in Cavan. The dispossessed natives instructed counsel to impugn the legality of the commissioners' action and Davies vindicated the justice of the proceedings in an oration wherewith the natives "seemed not unsatisfied in reason, though in passion they remained ill-contented, being grieved to leave their possessions to strangers, which their septs had so long after the Irish fashion enjoyed".

In a letter to Cecil, dated 29th July 1611, Davies again begged to be recalled. He had now more leisure time at his disposal and found time to write his learned and elaborate treatise, 'A Discovery of the True Causes why Ireland was never entirely Subdued, nor brought under Obedience of the Crown of England, until the Beginning of his Majesty's Happy Reign,' which was published in London in 1612, with a dedication to the King. Early in 1612, he came to England, on Irish business, and, on 20th April, finding that the arrangements for the holding of the Irish Parliament, which was to meet in November, would not be completed before midsummer, he begged Cecil to procure him permission to practice in the meanwhile in London. He was detained in London until the end of September. The day finally appointed for the opening of the Irish Parliament was 18th May 1613, on which day the members of the lower house assembled to elect a speaker. Sir Thomas Ridgeway proposed Davies, who had been returned for Fermanagh, as speaker, intimating that his appointment had been recommended by the King. Thereupon Sir James Gough, as champion of the Catholic party, proposed Sir John Everard, a noted lawyer and a recusant. During the scene of disorder that ensued, the Catholic members contrived to install Everard in the Speaker's Chair. As Everard refused to vacate the chair, Sir Oliver St. John and Ridgeway "took Sir John Davies by the arms, lifted him from the ground, and placed him in the chair, in Sir John Everard's lap, requiring him still to come forth of the chair". Eventually Everard was ejected from the chair and withdrew from the outer chamber, in the company of his ninety-eight supporters. When he had been formally presented to the Lord Deputy, on 21st May, and his election had been approved, Davies delivered a memorable speech in which he reviewed, at length, the history of Irish Parliaments. In the following September, commissioners of inquiry from England arrived in Dublin to consider the grievances of the Catholic members. One result of their inquiry was to confirm Davies' election to the Speaker's Chair. On the reassembling of the Irish Parliament, 11th October 1614, Davies delivered a congratulatory address to the members; and in the same year he was returned to the English Parliament as member for Newcastle-under-Lyme. He was associated at this time with Sir Robert Cotton and others in re-establishing the Society of Antiquaries. In 1615, was published in Dublin, 'The Primary Speeches in the Cases and Matters of the Resolutions & Adjudications of the Courts of the King of this Realm collected by Sir John Davies'. He continued to hold office until 30th October 1619, when he was succeeded by Sir William Ryves. On 21st June 1619, he had written to the Duke of Buckingham asking that Ryves might be appointed as his successor.

Sir John continued his professional practice as King's Sergeant in England and frequently went on circuit as a judge. In the parliament of 1621, he sat as member for Newcastle-under-Lyme again and occasionally spoke on Irish matters. In 1622, he collected in a single volume, some of his best known poems. His 'Abridgement of Sir Edward Coke's Reports' had first appeared in 1615; but his treatise, 'The Question concerning Impositions, Tonnage, Poundage, Prizage, Customs, etc' was not published until 1656. 

In 1623, Sir John retired to Englefield House in Berkshire which he had lately purchase from the moneylender, Sir Peter Vanlore. On 9th November 1626, Chief-Justice Crew was discharged from his office for refusing to countenance the legality of King Charles' forced loans. Davies, who had strenuously supported the new king's demands, was appointed his successor; but he never took possession of the office. On the night of 7th December 1620, he was at a supper-party given by Lord-Keeper Coventry and, on the morning of 8th December, he was found in his bed, dead of apoplexy. He was buried at St. Martin-in-the-Fields' Church at Charing Cross. His widow, a fanatical prophetess, remarried to Sir Archibald Douglas, but was buried by Sir John's side upon her own death in 1652. They had two sons, both of whom died young: one, who was dumb, drowned in Ireland. Their daughter, Lucy, and her husband, Ferdinando, Lord Hastings, later 6th Earl of Huntingdon, inherited the Davies estates. They sold up to the Marquis of Winchester in 1635.