The Ruthvens were involved in several plots against Mary, Queen of Scots, and King James VI, and eventually forfeited the castle in 1600.

Dirleton ceased to be a residence, although Oliver Cromwell was forced to besiege the castle to flush out a band of "mosstroopers" (marauders), during the Third English Civil War in 1650.

The damaged castle was then acquired by John Nisbet, Lord Dirleton, who decided to build a new country house on the nearby Archerfield Estate.

Only the basement levels survive of the 14th- and 15th-century additions built by the Haliburtons, although these comprised a large hall and tower house along the east range.

[6] The 13th-century stone castle, of which only the donjon, or keep, remains, represented a show of de Vaux's status, and would have required peaceful times to permit a prolonged construction project.

[8] Dirleton withstood the assault for several months, until the English victory at Falkirk allowed them to bring up large siege engines, after which the castle was soon reduced.

In the 1420s, Sir Walter Haliburton (d. before 1447) acted as a hostage in exchange for the release of King James I, who had been held captive by the English since 1406.

[8] King James IV visited Dirleton in September 1505, and gave money to the masons then engaged on works in the north-east part of the castle.

The son of William and Janet, Patrick, 3rd Lord Ruthven (c. 1520–1566), was one of the leaders of the group who murdered David Riccio, private secretary to Mary, Queen of Scots, in 1566.

[11] Patrick was forced to flee to England, where he died, leaving Dirleton to his son William (c. 1541–1584), who was created Earl of Gowrie in 1581.

Although Gowrie was pardoned the following year, he was executed in 1584 for his part in another plot to seize Stirling Castle, and his lands were forfeited to the crown.

[8] A keen amateur arboriculturalist, Lord Gowrie is thought to have laid out the gardens at Dirleton, and planted numerous trees.

[13] James VI granted Dirleton to the Earl of Arran, who entertained the King there for twelve days in May 1585, while there was plague in Edinburgh.

Dorothea Stewart and her new husband Andrew Kerr of Faldonsyde complained in 1597 about a group of local men who stole rabbits from the links of Dirleton and terrorised her tenants.

While this was happening at Gowrie House, the other two Ruthven brothers, William and Patrick, were at Dirleton, apparently unaware of the plot afoot.

[18] Oliver Cromwell's army invaded Scotland in 1650, during the Third English Civil War, and defeated the Scots Royalists at Dunbar on 3 September.

With this victory, Cromwell gained effective control of southern Scotland, but bands of Royalist moss-troopers continued to harry the English supply lines.

[26] The trial included being assessed by the 'witch pricker' John Kincaid, who searched for a part of the accused body which was not subject to pain, or other 'devil's mark' bodily signs to be used as evidence that they were indeed witches.

The trials took place in the Dirleton Castle Great Hall, and although the sentence and action taken do not survive either, those accused were usually executed, as required by law,[27] often by strangling.

[26] Nicola Sturgeon, the first minister of Scotland, issued an officially apology for the first time, for the persecution of alleged witches during the 16th, 17th, and 18th centuries.

The most substantial remains are the Ruthven Lodging, the gatehouse, and the de Vaux keep to the south, while only the basement of the east range survives.

Internally, the original use of the rooms is difficult to interpret,[4] although the round towers may have served as private suites for Lord Dirleton and his Lady.

[31] A room in the square tower to the west, possibly the lord's bedroom,[8] has holes in the ceiling to allow smoke from braziers to escape.

Although only the basement survives, this once formed one of the finest noble residences of its time in Scotland, and would have been similar to the contemporary buildings at Doune Castle.

Two large ovens and a well lie at the south end, while at the east is the 13th-century postern, blocked when the wall was thickened to support the new buildings above, and re-used as a fireplace.

[36] The three-storey building is constructed, like the Haliburton range, from undressed stone, although the Ruthven Lodging is decorated with string courses, horizontal mouldings running around the walls.

[37] West of the bowling green is a flower garden, laid out in 1993 to an 18th-century design, and containing yew, cedar, monkey puzzle and Lawson's cypress trees.

To the north is the 1920s Arts and Crafts garden, which is home to a 215-metre (705 ft) -long herbaceous border, and is overlooked by a castellated 19th-century gazebo, or summer house.

The rest of the gardens comprise lawns, with numerous mature specimen trees, including redwood, beech, and sycamore.

The doocot is 7.6 metres (25 ft) high, and contains around 1000 nesting boxes for pigeons, which were an important source of food for the castle's inhabitants.