He supported the government of the queen dowager, and in 1560 was one of the three nobles who voted in parliament against the Reformation and the confession of Faith, and declared their adherence to Roman ttholicism. Subsequently, however, he joined the league against Huntly, whom with Murray and Morton he defeated at Corrichie in October 1562, and he supported the projected marriage of Elizabeth with Arran.
On the arrival of Mary from France in 1561 he was appointed one of the twelve privy councillors, and on account of his religion obtained a greater share the queen's favour than either Murray or Maitland. He was one of the principal supporters of the marriage with Darnley, came the leader of the Roman Catholic nobles, and with mnox obtained the chief power in the government, successfully otecting Mary and Darnley from Murray's attempts to regain his ascendancy by force of arms. According to Knox he openly tended mass in the queen's chapel, and was especially trusted Mary in her project of reinstating Roman Catholicism. The fortress of Tantallon was placed in his keeping, and in 1565 he is made lieutenant of the north of Scotland. He is described e same year by the French ambassador as “très grand catholique hardi et vaillant et remuant, comme l'on dict, mais de nul"
After the murder of David Rizzio, in 1567, he Joined the Protestant lords against Mary, appeared as one of the leaders against her at Carberry Hill, and afterwards approved of her imprisonment at Lochleven Castle. In July he was present at the coronation of James, and was included in the council of regency to Mary's abdication. He, however, was not present at Langside in May 1568, and in July became once more a supporter of Mary, tic ting for her divorce from Bothwell (1569). In March 1570 he formed with other lords the joint letter to Elizabeth asking for the queen's intercession and supporting Mary's claims, and was present at the convention held at Linlithgow in April in opposition to the assembly of the king's party at Edinburgh.
In 1574 he was proceeded against as a Roman Catholic and threatened with excommunication, subsequently holding a conference with the ministers and being allowed till midsummer to overcome his scruples. He had failed in 1572 to prevent Morton's appointment to the regency, but in 1578 he succeeded with the earl of Argyll in driving him from office. On March 24, James took the government into his own hands and dissolved the regency, and Atholl and Argyll, to the exclusion of Morton, were made members of the council, while on the 29th Atholl be is appointed lord chancellor. Subsequently, on May 24, Morton succeeded in getting into Stirling Castle and in attaining his guardianship of James. Atholl and Argyll, who were now corresponding with Spain in hopes of assistance from that quarter, then advanced to Stirling with a large force, when a compromise was arranged, the three earls being all included in the government.
While on his way from a banquet held on April 20, 1579 on the occasion of the reconciliation, Atholl was seized with sudden illness, and died on the 25th, not without strong suspicions of poison. He was buried at St Giles's cathedral in Edinburgh. He married (1) Elizabeth, daughter of George Gordon, 4th earl of Huntly, by whom he had two daughters, and (2) Margaret, daughter of Malcolm Fleming, Lord Fleming, by whom, besides three daughters, he had a son, 5th earl of Atholl, at whose death in 1595 the earldom in default of male heirs reverted to the crown.
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