While the cemetery opened in 1855, the oldest human remains are the re-interred remains of three men from the fever ship Glen Huntly. Originally they were first buried at Point Ormond (now Elwood) in April 1840.

The three men, John Craig, George Armstrong and James Mathers, set off from Greenock, Scotland along with over 150 other new immigrants heading for the new colony which had been settled in Melbourne. Fever and diseases like typhoid struck throughout the journey. Ten immigrants died during the voyage. Upon entering Port Phillip the Glen Huntly was flying the yellow fever flag, causing much consternation amongst the settlers of Melbourne.

Victoria’s first quarantine station was hastily set up at Red Bluff Point Ormond. It was made up of two camps, one for the fever patients and one for those who were free from the disease. John Craig, George Armstrong and James Mathers died soon after and were initially buried at Point Ormond.

Enclosed by a picket fence, the graves remained for many years until it was noticed that the surrounding earth and rocks were being washed away by the sea. The bodies were exhumed and interred into a new grave at St Kilda Cemetery on the 27th August 1898 in the presence of St Kilda councillors and family members.

Ornamental entrance gates set back from the roadway in an arc formation were erected between 1900 and 1910. An historic palisade boundary fence was also placed along the Dandenong Road boundary. Both the boundary fence and entrance gates remain in place today.

During 1970, the caretaker’s lodge was removed to make way for the Michaelis Lawn burial area. Wall niches and a memorial rose garden for cremated remains were also established.

St Kilda Cemetery celebrated its sesquicentennial (150th) year in 2005 and this was marked by the commencement of a major redevelopment. The initial stages of the works provided the local community with an opportunity to re-commence use of the cemetery. New burial locations were made available for sale for the first time in over twenty years and a further 33 graves were released in 2007.