After standing trial in the Summer Court, James is sent on a quest to kill the Cait Sidhe, the monstrous faery cat who manipulated him into betraying the Seelie faeries and destroying the magical barrier that protected them. When the time comes to kill the beast, James decides to trick him into helping undo his mistake. But the man beneath the beast, Cecil Morris, is just as dangerous, and his manor, Heatherfield, is full of wild and deadly magic. In trying to reach Cecil, James risks being pulled into the darkness with him.

Cai, accompanying James to Heatherfield, escapes from the Cait Sidhe's prison and fights for his life against Heatherfield's deadly magic, determined to keep his oath to kill the beast even if it means making James his enemy. Kallista and Alan, also captives in the manor, face a fight of their own as Alan's Unseelie magic slowly consumes him.

Meanwhile, newly-appointed Noble Faery Deirdre and her human champion, Iain, head into an ancient tomb to find her drachma, an item that will help her control her powerful magic and save the Summer Court from destruction. She must undergo a trial to earn her drachma, but dark forces lurk inside, waiting to use her magic against her and against all she loves.

The Thrall's Gambit is book five in the seven-book Winter's Blight series.