Duckenfield, 75, has denied the manslaughter by gross negligence of 95 Liverpool supporters who died in the crush at Sheffield Wednesday’s ground on 15 April 1989.
The 96th victim, Anthony Bland, suffered brain damage and remained in a permanent vegetative state until he died in March 1993, the court heard.
This meant his death was out of the time to be classed as resulting from manslaughter.
Richard Matthews QC opened the prosecution’s case at Preston Crown Court on Thursday.
He said Duckenfield was a chief superintendent, or “very senior” South Yorkshire Police officer, who had “ultimate responsibility” for the police operation to secure the safety of 50,000 fans attending the match.
Mr Matthews QC continued: “It is the prosecution’s case that David Duckenfield’s failures to discharge this personal responsibility were extraordinarily bad and contributed substantially to the deaths of each of those 96 people who so tragically and unnecessarily lost their lives.”
A previous trial took place in January but was discharged after the jury was unable to return a verdict, the court was told.
Mr Matthews told the jury: “That task of deciding the case against Mr Duckenfield has now been passed to you.”
He also warned jurors not to be influenced by anything else they had seen or read, and told them: “No one else has the task that you have: no other court, inquiry, inquest, jury or person has or can determine what is entrusted solely to you to decide on the evidence you will hear in this court.”
Mr Matthews told the court each of the victims of the Hillsborough disaster died “as a result of the extraordinarily bad failures by David Duckenfield in the care he took to discharge his personal responsibility on that fateful day”.
He added: “It was so bad, so reprehensible, so blameworthy and unforgivable that it amounts to a gross failure.”
Mr Matthews told the court all of the 24,000 Liverpool fans were directed to the Leppings Lane end of the ground, where limited turnstiles served a bottleneck of a very large crowd, ahead of the 3pm kick-off.
Duckenfield agreed to requests to open an exit gate to the stadium after crushing built up outside the turnstiles before the match between Liverpool and Nottingham Forest, the court heard.
Once through exit gate C, spectators saw a tunnel marked “standing” which led to the central pens on the terrace where the fatal crush happened.
Mr Matthews said: “In short, once in and beyond gate C, the crowd was naturally drawn down the slope of the tunnel and into the confined area of the central pens, and David Duckenfield gave no thought to the inevitable consequence of the flood of people through gate C, nor did he make any attempt to even monitor what was occurring, let alone avert the tragedy.”
The youngest victim of the disaster was 10-year-old Jon-Paul Gilhooley, and the eldest was Gerard Baron, aged 67, the jury was told.
Ninety-four of the victims died on the day of the disaster, while Lee Nicol, aged 14, died two days later from his injuries.