The new flight route, via Windhoek in Namibia, makes the small British island in the South Atlantic reachable by air from South Africa in just six hours. The airport has been a colossal civil engineering challenge.
St. Helena, with just over 4,000 residents known as "Saints", is best known as the rocky outcrop where French emperor Napoleon Bonaparte saw out his final days.
After five years of construction, controversy and embarrassing delays due to high winds, the airport built at a cost of £285 million (318 million euros) finally opened for business. "It will bring in tourists and we will be able to get a better standard of living," said the island's governor Lisa Phillips.
The volcanic tropical island itself measures just 122 square kilometres (47 square miles) and is located almost exactly halfway between Africa and South America. The island had no suitable flat surface to construct the necessary 1,950 metre-long airstrip. Engineers were forced to chip away a mountain peak and fill in a valley to create enough of an even surface.
Because of high winds, Comair abandoned plans to operate the route with a Boeing 737, paving the way for AirLink's smaller Embraer 190 jet. The winds meant that the airport could not be opened in 2016 as originally planned with a ribbon-cutting by Prince Edward, Queen Elizabeth II's youngest son. The conditions made take-offs and landings much more difficult than expected and just weeks before the scheduled ceremony, it was cancelled and the airport became practically unused. After more than a year of test flights and studies, the decision was taken to use the Embraer 190.
The island will be served by a weekly service from Johannesburg costing about £800 return ($1,060). The average salary on St. Helena is just £7,280. "It's more expensive that a flight to London" from South Africa, said Jacqui Wilson, who saved up to take the "historic" flight. But on the personal side people are just so glad there is an airport. "Now we will be able to go home more often. Our family and friends will be able to visit, which is very great," said Catherine Man, the only veterinarian on the island. It is also hoped that the air link will help reduce the island's dependence on aid from London which cost the British taxpayer £53.5 million in 2015 alone.
Its isolated location meant it was chosen as a place of exile for those who suffered defeat at the hands of the British, with Napoleon held there from 1815 until his death in 1821. Several thousand Boer prisoners of war were also detained there at the start of the 20th century.
St. Helena was one of the world's most inaccessible locations. It has been only reachable by sea, a five-day voyage from Cape Town aboard a Royal Mail vessel that chugs along at a speed of just 15 knots (28 kilometres an hour). Every three weeks, the RMS St. Helena has been the islanders' link to the outside world, bringing a cargo of food, post, visitors and vehicles.
When the RMS St. Helena is retired from service next year, the island will become almost completely dependent on its airport. But with its Napoleonic heritage, rare birds and exotic plant life, hopes are high that the island will become a nirvana for curious travellers.