The shrine is one of the country's most sacred sites for Shia Muslims and has drawn millions of pilgrims from around the world.
The shrine has stood in various forms since 944, when it was built to house the tombs of two ninth century imams, considered successors to the Prophet Muhammad.
Ali al-Hadi, the tenth imam who died in 868 and his son Hassan al-Askari who died in 874, were buried at the end of a turbulent period during which Samarra was built as the new capital of the Abbasid empire, briefly taking over from Baghdad, then the largest city in the world.
But the continued and intense religious importance of the site is connected to the 12th and final imam, Muhammad al-Mahdi.
Known as the "Hidden Imam" Shias believe he went into hiding in 878 under the al-Askariya shrine to prepare for his eventual return among men.
According to Shia tradition, al-Mahdi will reappear one day to punish the sinful and restore justice to humanity.
For many years, a saddled horse and soldiers would be brought to the Samarra shrine every day to be ready for his return.
The shrine was extensively rebuilt as Samarra's influence withered over the centuries and power was restored to Baghdad.
Modern-day Samarra, a tough, Sunni-dominated town in the middle of the Sunni Triangle north of Baghdad, fills just a fraction of the enormous ancient city that once stood along the banks of the Tigris.
The latest remodelling of the shrine took place in the late 19th century, with the golden dome that was destroyed in Wednesday's bombing added in 1905.
Covered in 72,000 gold pieces and surrounded by walls of light blue tiles, the dome was a dominant feature of the Samarra skyline.
Despite being an active base of Sunni insurgents since the US-led invasion of Iraq in March 2003, the al-Askariya shrine had survived unharmed and largely unthreatened until Wednesday.
It managed to escape any damage when Samarra was retaken in the first major US and Iraqi combined offensive in October 2004, which was aimed at sweeping out the Sunni factions that had taken over the town.
Many other Iraqi archaeological sites have been badly scarred by US efforts to control the insurgency.
No group has taken responsibility for the destruction of the Samarra shrine but the attack was immediately followed by Shia reprisals against Sunni mosques.