The appointment follows the arrival in November of former Oracle Team USA general manager Grant Simmer as chief executive of the Portsmouth-based team.
Holroyd won the Cup with Emirates Team New Zealand in 2000 and was formerly the Technical Director at Softbank Team Japan for the 35th America's Cup campaign.
"I'm really excited to be working with Nick again. It's fantastic he's agreed to join the team," Ainslie said in a statement on Wednesday.
"Adding his skillset and experience to our technical line up has greatly strengthened our challenge to win the 36th Americas Cup."
Ainslie plans to challenge holders Emirates Team New Zealand for the next America's Cup in 2021.
The 40-year-old Briton and his crew failed in their first attempt to win the "Auld Mug" last year in Bermuda, where New Zealand trounced Oracle founder Larry Ellison's team in state-of-the-art foiling catamarans.
New Zealand get the right to choose what type of boat to sail in and have opted for a monohull design rather than the multihull catamarans used in Bermuda.
(Reporting by Alan Baldwin; editing by Alexander Smith)
