At the age of 13, James made his formal entry into Edinburgh. Upon arriving he met the 37-year-old, married, father of 5 children, Franco-Scottish lord Esmé Stewart, 6th Lord d'Aubigny, whom the Puritan leader Sir James Melville described as "of nature, upright, just, and gentle". The two became extremely close and it was said by an English observer that "from the time he was 14 years old and no more, that is, when the Lord Stuart came into Scotland... even then he began... to clasp some one in the embraces of his great love, above all others" and that James became "in such love with him as in the open sight of the people often he will clasp him about the neck with his arms and kiss him".
The King first made Aubigny a gentleman of the bedchamber. Later, he appointed him to the Privy Council and created him earl and finally duke of Lennox. In Presbyterian Scotland the thought of a Catholic duke irked many and Lennox had to make a choice between his Catholic faith or his loyalty to James. At the end Lennox chose James and the king taught him the doctrines of Calvinism. The Scottish Kirk remained suspicious of Lennox after his public conversion and took alarm when he had the earl of Morton tried and beheaded on charges of treason. The Scottish ministry was also warned that the duke sought to "draw the King to carnal lust".
In response the Scottish nobles plotted to oust Lennox. They did so by luring James to Ruthven Castle as a guest but then kept him as prisoner for ten months. The Lord Enterprisers forced him to banish Lennox. The duke journeyed back to France and kept a secret correspondence with James. Lennox in these letters says he gave up his family "to dedicate myself entirely to you"; he prayed to die for James to prove "the faithfulness which is engraved within my heart, which will last forever." The former duke wrote "Whatever might happen to me, I shall always be your faithful servant... you are alone in this world whom my heart is resolved to serve. And would to God that my breast might be split open so that it might be seen what is engraven therein."
James was devastated by the loss of Lennox. In his return to France, Lennox had met a frosty reception as an apostate Catholic. The Scottish nobles had thought that they would be proven right in their convictions that Lennox's conversion was artificial when he returned to France. Instead the former duke remained Presbyterian and died shortly after, leaving James his embalmed heart. James had repeatedly vouched for Lennox's religious sincerity and memorialized him in a poem called Ane Tragedie of the Phoenix, which likened him to an exotic bird of unique beauty killed by envy.