But its role in the wars in Iraq, Afghanistan and the Balkans, and in the hunt for Osama bin Laden, had been little recognised until one of its most senior spies broke ranks recently to pen a tell-all account.
Intelligence analyst David Rosenberg spent 18 years at the base, 20 kilometres (12.4 miles) south of Alice Springs, working with top-secret clearance for the National Security Agency (NSA), home to America's code-cracking elite.
Formally known as the "Joint Defence Space Research Facility", Pine Gap is one of Washington's biggest intelligence collection posts, intercepting weapons and communications signals via a series of satellites orbiting Earth.
Australia has had joint leadership at the post and access to all intercepted material since 1980, but the base's history is not without controversy.
Former prime minister Gough Whitlam was sensationally sacked by the British monarchy -- allegedly at American urging -- not long after he threatened to close Pine Gap in 1975, although other domestic political issues were also involved in his removal.
Its futuristic domes were originally built as a weapon in America's spy war with Russia, officially starting operations in 1970, but Rosenberg says it is now targeting the US-led "war on terror" and Asia's military boom.
"There's a large segment of the world that are weapons-producing countries who have programmes that the United States and Australia are interested in, and obviously a lot of Asia encompasses that area," Rosenberg told AFP.
The career spy is under a lifetime secrecy agreement with the NSA, meaning he cannot reveal classified information and is limited in what he can say about his time at Pine Gap, but said North Korea and China were among its targets.
"I think any country that has a large military, is a large weapons producer, is always going to be a focus for the intelligence community and China of course is growing and it's growing rapidly," he said.
"There are developments there that we are looking at."
India and Pakistan were also "very much of a concern", he added, with a surprise nuclear test by New Delhi in 1998 catching Pine Gap's analysts "blind".
The latter half of his time at the mysterious station known to locals as the "Space Base" was dominated by the wars in Iraq and Afghanistan and an intense focus on Al-Qaeda following the September 11 attacks in 2001.
Rosenberg recalls that day as his most sombre in the job, with analysts scouring the region for clues on what was going to happen next, knowing instantly that Al-Qaeda was responsible and fearing they would strike again.
"While these attacks were happening we of course were thinking how many other simultaneous or near-simultaneous actions are going to happen?" he said.
"We didn't know how many other attacks had been planned that day."
It was also a huge wake-up call to the fragmented spy community, he added, who soon realised all the signs had been there of an impending attack but they had failed to piece them together to perhaps prevent 9/11.
Delays also allowed Bin Laden and other Al-Qaeda leaders to escape into hiding, a "significant intelligence failure" which left agents with a 10-year hunt Rosenberg was not around to see completed -- one of his few regrets.
It was "certainly possible" that Pine Gap was involved in the US mission which ultimately saw Bin Laden killed in Pakistan in May, he added.
He sees "cyber-warfare" such as state-endorsed hacking and increasingly portable technology allowing, for example, the remote detonation of a bomb with a mobile phone, as the next big front for the intelligence community.
Rosenberg's book offers a rare insight into the mysterious world of military espionage, discussing widespread doubts amongst spies about the since-debunked claims of weapons of mass destruction that presaged the invasion of Iraq.
It was screened 16 times before publication by four intelligence agencies -- three American and one Australian -- and has been altered or blacked out in sections through an arduous censorship process which saw him, at one point, taken into a vault in Canberra for interrogation.
Defence officials were also due to seize and destroy his computer hard-drive to ensure classified elements of the original manuscript were wiped out.
But the self-confessed "Mission: Impossible" fan said he had no regrets about telling his story.
"Imagine being in a job where secrecy surrounds everything you did for 23 years -- it's kind of like letting the cork out of a champagne bottle, all the secrets come flowing out," he said."It was quite a liberating experience for me."