Ark Royal was originally built to order by the shipbuilder R. Chapman, of Deptford, for Sir Walter Raleigh, who was approximately 32 years of age at the time. The ship was to be called Ark, which became Ark Raleigh, following the convention at the time where the ship bore the name of her owner. The Crown, in the person of Queen Elizabeth I, purchased the ship from Raleigh in January 1587 for the sum of £5,000. She was henceforth to be known as Ark Royal.

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Her first action came in 1588 during the attack of the Spanish Armada, when Ark Royal, as one of the largest vessels in the English fleet, was the flagship of Lord High Admiral Howard. After the initial defeat of the Armada, Ark Royal led the chase of the fleeing ships into the North Sea and beyond the Firth of Forth. She was also used as Howard's flagship during the 1596 raid on Cádiz, which resulted in the destruction of much of the Spanish fleet at harbour. Ark Royal was the flagship once more during 1599 when a Spanish invasion again threatened.

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On the accession of James VI and I to the English throne, Ark Royal was renamed Anne Royal, after his consort, Anne of Denmark. She was then rebuilt at Woolwich Dockyard in 1608 by Phineas Pett I as a 42-gun royal ship. Under her new name, she was the flagship of Lord Wimbledon in the 1625 raid on Cádiz which ended in disaster due to inadequate preparation.

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She remained in service until April 1636, when she was being moved from the River Medway to serve as the flagship of Sir John Penington. While anchored in shallow water, she struck her own anchor and stove in her timbers, sinking in the river. She was raised at a cost greater than her original purchase price, but was found to be damaged beyond repair, and subsequently broken up in 1638.

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Her fame led to a number of later warships of the Royal Navy being named Ark Royal in her honour, including a number of flagships of the fleet.