Archaeologists working alongside National Trust for Scotland have been investigating the caves over the summer and unearthed remnants of the door for the first time.
Meanwhile, radiocarbon tests carried out on items found in the caves - which were famously used by smugglers in the 17th and 18th Century - indicate that the subterranean structures were occupied up to 1,800 years ago during the Iron Age.
Following the findings, NTS now hope to open up the castle caves to the wider public.
Derek Alexander, Head of Archaeological Services for NTS, said: “We are really excited about this discovery and the results of the excavation so far.
“We knew there was a wall and doorway at the mouth of the Castle Cave but there was nothing at the entrance of the Stables Cave. A couple of stones on the surface suggested there might have been a wall.
“Imagine our surprise when we found two sides of a doorway surviving up to 8 courses high buried to a depth of about one metre. The doorway is quite wide, measuring 1.1m across and could have been secured with a draw bar.
Charcoal found in the lowest midden deposit in the upper chamber of Castle Caves dates from between 135 and 325 AD, according to radiocarbon testing.
Mr Alexander added: “This is similar to a date from the Gazebo Court on top of the cliff above the cave but is the earliest dated evidence from the caves.
“Uncovering new finds like this helps us to inspire others to support us in our work to ensure Scotland’s heritage is valued by everyone and protected now and for future generations.”
The finds were made during a Thistle Camp which give volunteers a chance to work on archaeological and conservation projects at Scotland’s historic sites.
Christine McPherson, Thistle Camp leader said: “We found lots of modern pottery, glass and some 18th century wine bottles. An iron strip may have been part of the door hinge or fittings.”
Lucas Merz, a volunteer from Berlin, said: “I’ve never done archaeology before. It has been a great experience. Working in the caves is very special.”
Culzean Castle and Country Park, on the coast near Ayr, was home to the Kennedy family for generations and is one of the most popular tourist attractions in Scotland.
However, few visitors are aware that the famous castle was built over a warren of caves, NTS said.
One set of caves sits below the Stables and is open to the public while the caves below the castle are sealed with a stone frontage and barred entrances.
Ian Cornforth, Culzean Head Ranger said: “These results will help inform our interpretation of the Culzean and the human activity in the caves. There are so many stories to tell here and share with our visitors.”