The Californication star will portray a fairy named Claudette, a sister of Claude (Giles Matthey) who imparts her wisdom on Sookie (Anna Pacquin).
Luddington achieved fame for playing Catherine, Duchess of Cambridge in the Lifetime movie William & Kate, which aired in the run-up to the royal wedding last April.
Child star Jacob Hopkins became the latest addition to the True Blood cast in February.
Other stars to have signed up for roles include Law & Order: SVU's Christopher Meloni and Spartacus actor Peter Mensah.
True Blood showrunner Alan Ball has announced that he will step down from the show after its fifth season, which premieres on HBO in the summer.