In 1541, King Henry was about to wage a war against the French. A plan was made to use Folkestone as a port of embarkation to supplies and troops. He sent a Master Tuk and Master Captain of Sandgate to look for a site for the new harbour. Plans were made but never implemented. On 2 May 1542, the king came to Folkestone but then headed to Dover on 6 May. The Folkestone Harbour plan was abandoned.

In 1804, the Earl of Radnor had petitioned Parliament for the construction of a stone harbour. In 1807, an Act of Parliament was passed to build a pier and harbour, which was built by Thomas Telford in 1809. In 1810, the new harbour of local sandstone was complete. By 1820, a harbour area of 14 acres (5.7 hectares) had been enclosed. Folkestone’s trade and population grew slightly but development was still hampered by sand and silt from the Pent Stream. The Folkestone Harbour Company invested heavily in removing the silt but with little success. In 1842, the company became bankrupt and the government put the derelict harbour up for sale. It was bought by the South Eastern Railway (SER), which was then building the London to Dover railway line, and from June 1843 was the base for a ferry service to Boulogne, after a successful trial by the steam packet Water Witch. George Turnbull was responsible in 1844 for building the Horn pier.

During World War II, the port closed to civilian boat usage and 44,000 personnel used the port during the Dunkirk Evacuation, filling up to eighty trains heading to London. In 1945, cargo services returned to the harbour and ferries went to Calais and Belgium. On 1 August 1946, the SS Auto Carrier started carrying cars to Boulogne. July 1947 the Folkestone-Boulogne service resumed after a winter break. Over 67,000 passengers had used the service.

In 1960, the services were very popular and were carrying over 800,000 passengers, 438 cars and 276 lorries or commercial vehicles. In 1971-2, a roll-on/roll-off ramp was built for two new ships, Hengist and Horsa. By 1972, the Folkestone to Boulogne, Calais and Ostend services were carrying up to 1,266,783 passengers, 913,160 cars, 5,633 commercial vehicles and 31,594 freight vehicles (lorries and trucks).

In 2001, all ferry services stopped. During this time, the fishing industry was going through various changes and by 2002, only ten boats (with thirty men) were employed in the fishing industry.

In 2010 a plan was commissioned for the development of the harbour and seafront from architect Sir Terry Farrell and Partners, and outline planning permission was granted in the summer of 2013. Clearance of redundant and dilapidated buildings took place in 2014/15, and stonework and original steelwork on the harbour arm have been carefully restored so that the area can be opened up to the public as a new pier and promenade from the summer of 2015. Much of the former fairground site is being used for car parking and temporary recreational use whilst preparations continue for the rest of the development.