US researchers used CT scans to build a computer model of what Helicoprion looked like and how it ate.
They were also able to resolve an ongoing puzzle over whether the unique saw-like spirals were located inside or outside the mouth.
The findings show the animals were more closely related to modern chimaeras, or ratfish, than sharks.
The study is published by researchers from Idaho State University in the Royal Society journal Biology Letters.
The university's Museum of Natural History has the largest public collection of fossilised Helicoprion in the world.
The fish lived 270 million years ago but because they were largely formed from cartilage, which does not preserve well, their fossil record comprises unusual spiral structures.
Early theories suggested that they were actually used for defence and were located on the fish's upper or lower jaws, or even the dorsal fin.
Dental records
To solve the mystery, Dr Leif Tapanila and colleagues investigated the most complete fossil in the collection.
The fossil, discovered in Idaho, has a whorl measuring 23cm with 117 individual teeth. Unlike other specimens, the fossil also includes impressions of the cartilage structures.
The team used a high-powered CT scan, which uses X-rays to create a detailed computer image, in order to fully analyse what was inside the rock.
"When we got the images back, we could easily see that we had the upper and lower jaw of the animals, as well as the spiral of teeth," said Dr Tapanila.
"For the first time we were able to very clearly image how that spiral of teeth relates to the jaw."
The scientists found that the spiral was connected to the fish's lower jaw, in the back of the mouth.
"Imagine that... instead of having a tongue, you have this large spiral of teeth," Dr Tapanila explained.
"Only maybe a dozen teeth are poking up out of your lower jaw so you can bite."
"The rest of those teeth are stored inside and are not being used, those are your baby teeth - the teeth you had when you were younger."
Using the computer images, the team could build a 3D model of the jaw, to reveal how the tooth spiral worked.
"As the mouth closes, the teeth spin backwards... so they slash through the meat that they are biting into," Dr Tapanila reported.
"The teeth themselves are very narrow: nice long, pointy, triangular teeth with serrations like a steak knife.
"As the jaw is closing and the teeth are spinning past whatever it's eating, it's making a very nice clean cut."
Of the 100 fossils of Helicoprion that have been discovered, very few show broken or worn teeth.
Ancient diet
Dr Tapanila said that this evidence, combined with the "rolling and slicing" mechanism, provided clues to what the ancient fish ate.
"If this animal were eating other animals that were very hard or [had] hard armour plating or dense shells, you would expect more damage to their teeth.
"This leads us to believe that our animal was probably eating soft, squishy things like calamari. It was probably eating squid or its relatives that were swimming in the ocean at the time."
The study also highlighted the family connections of the ancient fish, categorising it with chimaeras and ratfish rather than sharks.
"One of the main ways that fish are identified is based on how the upper jaw connects to the rest of the skull," said Dr Tapanila.
"Because we have the upper jaw we can look at the bumps and grooves on it and see how it would have connected.
"It was fixed in two positions and was fused essentially to the brain tip... a feature that's distinctive for chimaeras and ratfish."
Following the reconstruction the jaw of the fish, the team is using inferred characteristics to create a scale model of the 4m animal for an exhibition at the Idaho State University Museum of Natural History this summer.
Based on fossil evidence, scientists believe the fish could have measured up to 7.6m long.
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