The Olympic champion's team Ben Ainslie Racing (BAR) hopes to be the first British challenger to win the trophy.
A four-day event in the city will open with a sailing parade later, with racing taking place at the weekend.
Six teams will battle it out at regattas around the world ahead of the final races in 2017.
Events have also been scheduled in Gothenberg, Sweden, in August, and Bermuda in October.
Four to six regattas are expected in 2016, including a second event in Portsmouth in July.
Defenders Oracle Team USA - which Ainslie helped to win the cup in 2013 - will take part, as well as crews from Sweden, France, New Zealand and Japan.
Their overall placement will affect the seeding and starting score they take into the America's Cup qualifier events in 2017.
Following the opening ceremony in Portsmouth later, practice racing will follow on Friday when teams will familiarise themselves with the race course.
Competition takes place on Saturday and Sunday, culminating in the "Super Sunday racing showdown".
The event is expected to attract up to 500,000 spectators.
A race village has been set up in Southsea Common and will provide a free viewing platform and large screens during the event.
Organisers said the course is "amazingly close to shore". There will also be an on-water spectator area for small boats.
•First staged in 1851 off the Isle of Wight in England and won by US yacht America
•No British team has won it in its 164-year history
•Racing is boat-on-boat, called match-racing
•Takes place roughly every three to five years
Sir Ben Ainslie will begin Britain's bid to win the 35th America's Cup as the opening leg of the series gets under way in Portsmouth.