[1] Leslie took an active part with the Lords of the Congregation, first against the queen-mother, Mary of Guise, when she was regent of Scotland, and afterwards against Mary, Queen of Scots in opposing her marriage with Lord Darnley, and in being part of the plot to murder David Rizzio.

He was, however, one of the peers who acquitted Bothwell of Darnley's murder, and went over to the side of the queen.

[2] As the Marian civil war continued, in April 1573, Rothes negotiated for Regent Morton and the King's party with the "Castilians" William Kirkcaldy of Grange and Henry Echlin of Pittadro, who held Edinburgh Castle.

[3][4] Rothes continued to occupy a position of some prominence in Scottish affairs until his death in 1611.

A dispensation was required for the marriage, which cost Regent Arran £20 and he paid a dowry of £1,333 Scots.