[2] Cunningham would eventually enjoy a good relationship with the king, but his association with Regent Morton initially made him suspect.

[2] He was also under pressure from the a large section of the Scottish church, which was becoming more hostile to episcopacy; in 1586, the General Assembly accused him of adultery, a charge which the king cleared him of in 1587.

Cunningham gave a speech outlining the genealogy of the prince, his English descent, and the recent history of the diplomatic relations of Scotland.

[8] Cunningham's speech was problematic for its reference to the English succession, reminding the audience of a controversial poem by Andrew Melville, Principis Scoti-Brittanorum Natalia{{.

[10] In 1598, he was sent as a diplomat with Peter Young to Denmark and Germany to promote King James' claims to the throne of the Kingdom of England.