Every such victory makes it harder for citizens to prevail when they believe they have been mistreated by police officers. It also adds obstacles for the Justice Department’s own civil rights investigators when alleging police misconduct. That has led to some tense debates inside the department, current and former officials say, as the government’s civil rights and appellate lawyers discussed when the department should weigh in, and on which side. Those debates have led the Justice Department to take more nuanced positions than government lawyers might have otherwise, the officials said.

Image Teresa Sheehan sued after she was shot by San Francisco officers in 2008. The Justice Department backed the police. Credit... Patricia C. Sheehan, via Associated Press

“Law enforcement officers are routinely called upon to face grave dangers and to make often-unheralded sacrifices, and the law must give them the room to make real-time judgments to protect public safety,” said Emily Pierce, a Justice Department spokeswoman. “At the same time, building trust between law enforcement and the communities they serve and protecting human life and human dignity requires accountability for law enforcement officers. The department recognizes — and is committed to striking — that balance.”

Mr. Holder has called the civil rights division the crown jewel of the department, and it has rarely had such a high profile. Even before it garnered national attention with a scathing rebuke of the Ferguson Police Department after the fatal shooting of an unarmed black teenager by a white officer last summer, the division issued similar reports on other departments, including those in Seattle, Albuquerque, Newark and New Orleans.

Those efforts, along with deeply personal remarks from Mr. Holder about racial profiling, have drawn criticism from police officers who say he has not supported them. But Darrel W. Stephens, the executive director of the Major Cities Chiefs Association, said many officers probably did not know how often Mr. Holder’s Justice Department stood with them at the Supreme Court. “He’s sincere,” Mr. Stephens said. “He is supportive of the police.”

Private civil rights lawyers, though, have been frustrated that the Justice Department’s aggressive stance in civil rights reports does not extend to its positions before the Supreme Court. “A report can have an impact on a department for a time,” said Gary Smith, the lawyer for the driver in the Arkansas case. “But case law touches every officer in every department in the country.”

Eventually, he predicted, police departments facing civil rights investigations will challenge the Justice Department on its apparently contradictory positions. “You’re telling the Supreme Court it’s O.K., and you’re doing this to us?” Mr. Smith said.