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 Sir 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 disaster at the Liverpool v Nottingham Forest match, held at Sheffield Wednesday's ground, concluded the fans had been unlawfully killed.
The inquests found that Liverpool supporters were not responsible for the dangerous situation at the Leppings Lane turnstiles.
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.
An application will be made to the High Court in a matter of weeks and a senior judge will make a ruling in due course.
The full list of individuals and charges are:
The six men charged over Hillsborough
Hillsborough: Criminal charges explained
The defendants, other than Mr Duckenfield, will appear at Warrington Magistrates' Court on 9 August.
No organisation will face corporate charges and no-one from the ambulance service will be charged, said Sue Hemming, head of special crime and counter-terrorism at the CPS.
She explained that Sheffield Wednesday is now a "different company" and, as it is not a successor organisation, is not criminally liable for any offences that might have been committed in 1989.
Â£56.5m
cost of Operation Resolve
Â£42m
cost of IPCC investigation
17,000 lines of inquiry by Operation Resolve
11,000 statements taken by Operation Resolve
190,000 documents reviewed by IPCC investigation
23,000 images reviewed by IPCC investigation
The CPS brought charges following referrals from the Operation Resolve investigation into the causes of the disaster and the Independent Police Complaints Commission (IPCC) probe.
Assistant Commissioner Rob Beckley, from Operation Resolve, said: "Our inquiry looked at all aspects of the event, including the planning and the preparation for the game, the safety of the stadium and the response by the emergency services."
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.
Ms Hemming made the announcement of the intended prosecutions 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."
Campaigner Trevor Hicks, whose daughters Victoria, 15, and Sarah, 19, died in the disaster, said: "There will be six people facing criminal charges who might not have done if we hadn't been resilient and all stuck together and fought this long fight.
"There are no winners in this, it doesn't bring anybody back.
"What it does do is send a message about accountability, as we keep saying, that nobody but nobody is above the law; be it the police or anybody else."
Chairwoman of the Hillsborough Family Support Group, Margaret Aspinall, whose son James, 18, was killed, said: "This is definitely the start of the end.
"I think everybody needs that, I think we all need peace from Hillsborough but we can never have peace until we've got truth, justice, accountability.
"I think that's the time we'll all have peace."
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 sad that her brother who campaigned for years and died during the new inquests 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."
BBC News profiles of all those who died
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 offered a "tribute to all of those that spent a great deal of time trying to ensure there was justice for those that died at Hillsborough".
Dr Alan Billings, the South Yorkshire police and crime commissioner, said he hoped the start of criminal proceedings would "lead to a measure of closure for the family members who have experienced a long and traumatic process".
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."
Mr Metcalf declined to comment.
Former Ch Supt David Duckenfield faces 95 charges of manslaughter and five other senior figures will be prosecuted over the 1989 Hillsborough disaster.