One of the two snapshots depicts Collins in a touring car outside a hotel in Bandon taken just hours before his death.
The second captures the scene at Béal na mBláth on Aug 23, 1922, the day after the ambush, and shows what historians believe to be Collins’ shirt collar on the road.
No known photograph of the post-ambush site was believed to exist previously.
The photographs were taken by then 18-year-old Agnes Hurley, from Mallowgaton in Bandon.
Her remarkable collection spans 20 years from 1921, and includes hundreds of photographs. Part of the collection was lost but was rediscovered in an attic in Dublin last year.
Ms Hurley’s niece, Mim O’Donovan, from Bandon, brought the pictures to the Revolutionary Decade Roadshow in Clonakilty organised by the History Department at University College Cork on Saturday.
“Aggie went to Béal na mBláth to see what had happened because they’d heard gunshots the previous day. She was well informed of current affairs and if something was happening she would be there.
“She took hundreds of photographs over the years and she dated the back of every single one,” Ms O’Donovan said.
Designed to bring previously undocumented memorabilia from private ownership into the public domain, the roadshow event yielded unexpected results.
Modern history lecturer at UCC, Gabriel Doherty, said he is unaware of any other such photograph.
“I haven’t come across any photograph of the Béal na mBláth ambush site the following day, let alone one that shows an artifact from Collins left there,” he said.
Cork city and county archivist Brian Magee described the find as “extraordinary”.
“The attached story tells of blood on the ground, though it’s difficult to tell because its black and white. The fact that it survived is remarkable,” he said.
The photos will be scanned and archived to form part of the public record of a crucial period in Irish history.
Almost 200 people turned up with items of interest from the period 1912-1923 and family members connecting stories were recorded.
The roadshow aims to gather raw material to offer greater insight into the period ahead of a series of commemorative events beginning next year to mark the centenary of the 1913 Lockout.