The tin was used by Peter and Helen Kroger who, in 1961, were among five people accused of spying for the Soviet Union by selling secrets of Britain’s first nuclear submarine.
The item will form part of an exhibition, along with photographs covering police investigations and other artefacts, set to open at the Museum of London on 9 October.
The Crime Museum Uncovered will showcase objects gathered by police over the past 140 years.
Previously, only invited guests such as Sherlock Holmes author Sir Arthur Conan Doyle have been allowed access to the Metropolitan Police collection.
The talcum-powder tin is one of a series of ordinary items containing secret compartments used to hide microfilm that were found at the Kroger’s home in Middlesex.
Other objects used by the spy ring included batteries and cigarette lighters, explained a Museum of London spokeswoman.
‘These will also be on display, along with X-ray images showing secret compartments inside.’
The Krogers were given 20-year sentences after running their clandestine operations from an unassuming bungalow in Ruislip.
A shopping bag carried by one of the group was found to contain a tin of undeveloped film that revealed details of HMS Dreadnought, Britain’s first nuclear submarine.
When police arrived at the Krogers’ home, they discovered that a bathroom had been converted to double as a photographic darkroom and a loft housing more camera equipment, according to a BBC account of the case.
The then Attorney-General, Sir Reginald Manningham-Buller QC, said at the time: ‘I would suggest that here was the hub of a spy ring and, in view of the money found there, the bank of a spy ring.’
A neighbour recalled how Helen Kroger owned a large, expensive camera – a rarity in 1950s Britain.
But Helen Kroger was said to be a poor photographer, ‘forever missing off your head or just photographing feet’.
Peter and Helen Kroger were later unmasked as US citizens Morris and Lona Cohen.
The Krogers were released from prison in 1969 in exchange for British spy Gerald Brooke.
The Crime Museum Uncovered will run at the Museum of London until 10 April 2016.