Mr Duckenfield was match commander at the FA Cup semi-final when 96 Liverpool fans were fatally injured in a crush.
Ex-South Yorkshire Police (SYP) Ch Insp Norman Bettison, two officers, a solicitor and a Sheffield Wednesday club secretary also face charges.
The Prime Minister said it would be a day of "mixed emotions" for families.
Last year, new inquests into the 1989 disaster at the Liverpool v Nottingham Forest match in Sheffield concluded the fans had been unlawfully killed.
For legal reasons, Mr Duckenfield cannot be charged over the death of the 96th victim Tony Bland, as he died four years after the disaster, prosecutors said.
The Crown Prosecution Service (CPS) must apply to the High Court to lift an order imposed after he was prosecuted privately in 1999, which must be removed before he can be charged.
The full list of individuals and charges are:
Mr Duckenfield faces manslaughter by gross negligence of 95 men, women and children
Sir Norman faces four charges of misconduct in a public office relating to alleged lies he told in the aftermath about the culpability of fans
Graham Mackrell, former Sheffield Wednesday club secretary, will be accused of breaching Health and Safety and Safety at Sports Ground legislation
Peter Metcalf, who was a solicitor acting for SYP, is charged with perverting the course of Justice, relating to changes to witness statements
Former Ch Supt Donald Denton and former Det Ch Insp Alan Foster are accused of perverting the course of justice
No organisation will face corporate charges. No-one from the ambulance service will face charges, CPS chief Sue Hemming revealed earlier.
Who were the 96 victims?
The defendants, other than David Duckenfield who now lives in Ferndown in Dorset, will appear at Warrington Magistrates' Court on 9 August.
Ms Hemming made the announcement to victims' families at a private meeting in Warrington earlier.
She said: "Following our careful review of the evidence, in accordance with the Code for Crown Prosecutors, I have decided that there is sufficient evidence to charge six individuals with criminal offences.
"Criminal proceedings have now commenced and the defendants have a right to a fair trial."
The CPS brought charges following referrals from the Operation Resolve (OR) investigation into the causes of the disaster and the Independent Police Complaints Commission (IPCC) probe.
The IPCC investigated the conduct of both SYP and West Midlands Police (WMP) in the days and weeks afterwards.
Any decision regarding WMP, which was brought in to carry out the original investigation into the conduct of SYP officers, will be made at a later date.
The investigations
The OR inquiry followed 17,000 lines of inquiry and took 11,000 statements, costing £56.5m
The IPCC has reviewed 190,000 documents and 23,000 images at a cost of £42m
A further IPCC file on the conduct of WMP still needs "additional investigative work"
Barry Devonside, whose son Christopher, 18, was killed in the disaster, said: "Everybody applauded when it was announced that the most senior police officer on that particular day will have charges presented to him."
Evelyn McDonnell Mills, whose brother Peter McDonnell, 21, died, said she was "really happy", but added she was sad her brother, who campaigned for years, died in the first year of the new inquests and never got to see their conclusion.
Pete Weatherby QC, who represents 22 of the victims' families, said they had "always known that accountability is the most difficult objective".
"They remain keen to see the criminal process properly pursued for those who have been charged and given that, the rights of the defendants should be respected.
"They do however hope that the memories of their loved ones and the integrity of the fans who attended Hillsborough will be respected during the process."
At Prime Minister's Questions, Theresa May said: "I know from working closely with the families when I was home secretary that this will be a day of mixed emotions for them."
Labour leader Jeremy Corbyn said: "I think we should pay tribute to all of those that spent a great deal of time trying to ensure there was justice for those that died at Hillsborough."
SYP Chief Constable Stephen Watson said: "Decisions concerning the bringing of criminal charges are rightly for the CPS.
"Given that criminal proceedings are now active, it would be inappropriate for me to comment further for fear of jeopardising this important process in any way."
Dr Alan Billings, SYP Crime Commissioner, said: "The start of criminal proceedings against these individuals will hopefully lead to a measure of closure for the family members who have experienced a long and traumatic process."
A spokesman for Sheffield Wednesday said the club had no comment to make.
Mr Duckenfield and Mr Denton's legal representative Ian Lewis, from JMW Solicitors, said: "In light of the decision by the Crown Prosecution Service to commence criminal proceedings against David Duckenfield and Donald Denton, it would be inappropriate for me as their solicitor, or for my clients themselves, to make any comment."
- hero@gettyimages
- hero@gettyimages
