It has been the second most populated commune in Île-de-France after Paris since 1 January 2025, following the absorption of Pierrefitte-sur-Seine to its north, as passed by both municipal councils on 30 May 2024.

[3] Until the 3rd century, Saint-Denis was a small settlement called Catolacus or Catulliacum, probably meaning "estate of Catullius", a Gallo-Roman landowner.

Shortly after 250 AD, his grave became a shrine and a pilgrimage centre, with the building of the Abbey of Saint Denis, and the settlement was renamed Saint-Denis.

In 1793, during the French Revolution, under the dictatorship of Robespierre, Saint-Denis was renamed Franciade in a gesture of rejection of religion.

Around 475 AD, Sainte Geneviève had a small chapel erected on Denis' tomb, which by then had become a popular destination for pilgrims.

Dagobert granted many privileges to the monastery: independence from the bishop of Paris, the right to hold a market, and, most importantly, he was buried in Saint-Denis; a tradition which was followed by almost all his successors.

He also started the work of enlarging the Basilica of Saint Denis that still exists today, often cited as the first example of high early Gothic Architecture.

King Louis XIV (1638–1715) started several industries in Saint-Denis: weaving and spinning mills and dyehouses.

The remains were removed from the tombs and thrown together; during the French Restoration, since they could not be sorted out anymore, they were reburied in a common ossuary.

On that occasion, the commune of La Chapelle-Saint-Denis was disbanded and divided between the city of Paris, Saint-Denis, Saint-Ouen, and Aubervilliers.

The 1998 FIFA World Cup provided an enormous impulse; the main stadium for the tournament, the Stade de France, was built in Saint-Denis, along with many infrastructural improvements, such as the extension of the metro to Saint-Denis-Université.

On 13–14 November 2015, Saint-Denis was the main location of a series of mass shootings and hostage-takings just outside the Stade de France.

Paris Métro Line 12: Paris Métro Line 13: Tramways in Île-de-France: Regional Rail: Saint-Denis has a comparatively higher crime rate than most surroundings communes, with higher rates of robbery, drugs offences and murder.

[13] In 2010 Saint-Denis had the highest rate of violent crime in France with 1,899 violent robberies and 1,031 assaults (an average of six robberies and three assaults per day)[14] To fight insecurity and delinquency, the Minister of Public Safety Jean-Marc Ayrault increased national police force in the Basilica district and the Landy Nord, classifying them as a Priority Security Zone 'ZSP' since 2012.

[16][17] Saint-Denis made international headlines for violent disorder before and after the 2022 UEFA Champions League Final, in which fans of visiting football team Liverpool F.C.

[23] Saint-Denis has one private elementary, middle, and high school (Ensemble Scolaire Jean-Baptiste de la Salle-Notre Dame de la Compassion) and one private middle and high school (Collège et lycée Saint-Vincent-de-Paul).

[22][23] Saint-Denis is twinned with: The 2018 video game Red Dead Redemption 2 features a major city named Saint Denis, located in the fictional American state of Lemoyne.