diff --git a/Cargo.lock b/Cargo.lock
index 2f4f2eb3bf..3f6b7851d4 100644
--- a/Cargo.lock
+++ b/Cargo.lock
@@ -1826,6 +1826,7 @@ dependencies = [
  "futures 0.3.31",
  "git2",
  "gix",
+ "glob",
  "indexmap",
  "indoc",
  "insta",
diff --git a/cli/Cargo.toml b/cli/Cargo.toml
index 57be178226..a2d3400a91 100644
--- a/cli/Cargo.toml
+++ b/cli/Cargo.toml
@@ -64,6 +64,7 @@ dunce = { workspace = true }
 futures = { workspace = true }
 git2 = { workspace = true }
 gix = { workspace = true }
+glob = { workspace = true }
 indexmap = { workspace = true }
 indoc = { workspace = true }
 itertools = { workspace = true }
diff --git a/cli/src/commands/commit.rs b/cli/src/commands/commit.rs
index 2e79432958..52f75a4441 100644
--- a/cli/src/commands/commit.rs
+++ b/cli/src/commands/commit.rs
@@ -12,7 +12,7 @@
 // See the License for the specific language governing permissions and
 // limitations under the License.
 
-use clap_complete::ArgValueCandidates;
+use clap_complete::ArgValueCompleter;
 use jj_lib::backend::Signature;
 use jj_lib::object_id::ObjectId;
 use jj_lib::repo::Repo;
@@ -44,7 +44,7 @@ pub(crate) struct CommitArgs {
     /// Put these paths in the first commit
     #[arg(
         value_hint = clap::ValueHint::AnyPath,
-        add = ArgValueCandidates::new(complete::modified_files),
+        add = ArgValueCompleter::new(complete::modified_files),
     )]
     paths: Vec<String>,
     /// Reset the author to the configured user
diff --git a/cli/src/commands/diff.rs b/cli/src/commands/diff.rs
index 0f79aa707c..b3a1c28409 100644
--- a/cli/src/commands/diff.rs
+++ b/cli/src/commands/diff.rs
@@ -13,6 +13,7 @@
 // limitations under the License.
 
 use clap_complete::ArgValueCandidates;
+use clap_complete::ArgValueCompleter;
 use itertools::Itertools;
 use jj_lib::copies::CopyRecords;
 use jj_lib::repo::Repo;
@@ -59,7 +60,7 @@ pub(crate) struct DiffArgs {
     /// Restrict the diff to these paths
     #[arg(
         value_hint = clap::ValueHint::AnyPath,
-        add = ArgValueCandidates::new(complete::modified_revision_or_range_files),
+        add = ArgValueCompleter::new(complete::modified_revision_or_range_files),
     )]
     paths: Vec<String>,
     #[command(flatten)]
diff --git a/cli/src/commands/interdiff.rs b/cli/src/commands/interdiff.rs
index dbe2db66b3..d577e22bdf 100644
--- a/cli/src/commands/interdiff.rs
+++ b/cli/src/commands/interdiff.rs
@@ -16,6 +16,7 @@ use std::slice;
 
 use clap::ArgGroup;
 use clap_complete::ArgValueCandidates;
+use clap_complete::ArgValueCompleter;
 use tracing::instrument;
 
 use crate::cli_util::CommandHelper;
@@ -44,7 +45,7 @@ pub(crate) struct InterdiffArgs {
     /// Restrict the diff to these paths
     #[arg(
         value_hint = clap::ValueHint::AnyPath,
-        add = ArgValueCandidates::new(complete::interdiff_files),
+        add = ArgValueCompleter::new(complete::interdiff_files),
     )]
     paths: Vec<String>,
     #[command(flatten)]
diff --git a/cli/src/commands/resolve.rs b/cli/src/commands/resolve.rs
index 76bd8315a3..bd29479ab1 100644
--- a/cli/src/commands/resolve.rs
+++ b/cli/src/commands/resolve.rs
@@ -15,6 +15,7 @@
 use std::io::Write;
 
 use clap_complete::ArgValueCandidates;
+use clap_complete::ArgValueCompleter;
 use itertools::Itertools;
 use jj_lib::object_id::ObjectId;
 use tracing::instrument;
@@ -64,7 +65,7 @@ pub(crate) struct ResolveArgs {
     // TODO: Find the conflict we can resolve even if it's not the first one.
     #[arg(
         value_hint = clap::ValueHint::AnyPath,
-        add = ArgValueCandidates::new(complete::revision_conflicted_files),
+        add = ArgValueCompleter::new(complete::revision_conflicted_files),
     )]
     paths: Vec<String>,
 }
diff --git a/cli/src/commands/restore.rs b/cli/src/commands/restore.rs
index 11ec1bfdf7..5262dd6e3d 100644
--- a/cli/src/commands/restore.rs
+++ b/cli/src/commands/restore.rs
@@ -15,6 +15,7 @@
 use std::io::Write;
 
 use clap_complete::ArgValueCandidates;
+use clap_complete::ArgValueCompleter;
 use jj_lib::object_id::ObjectId;
 use jj_lib::rewrite::restore_tree;
 use tracing::instrument;
@@ -47,7 +48,7 @@ pub(crate) struct RestoreArgs {
     /// Restore only these paths (instead of all paths)
     #[arg(
         value_hint = clap::ValueHint::AnyPath,
-        add = ArgValueCandidates::new(complete::modified_range_files),
+        add = ArgValueCompleter::new(complete::modified_range_files),
     )]
     paths: Vec<String>,
     /// Revision to restore from (source)
diff --git a/cli/src/commands/split.rs b/cli/src/commands/split.rs
index e750af8705..25d2f01cf3 100644
--- a/cli/src/commands/split.rs
+++ b/cli/src/commands/split.rs
@@ -14,6 +14,7 @@
 use std::io::Write;
 
 use clap_complete::ArgValueCandidates;
+use clap_complete::ArgValueCompleter;
 use jj_lib::object_id::ObjectId;
 use jj_lib::repo::Repo;
 use tracing::instrument;
@@ -68,7 +69,7 @@ pub(crate) struct SplitArgs {
     /// Put these paths in the first commit
     #[arg(
         value_hint = clap::ValueHint::AnyPath,
-        add = ArgValueCandidates::new(complete::modified_revision_files),
+        add = ArgValueCompleter::new(complete::modified_revision_files),
     )]
     paths: Vec<String>,
 }
diff --git a/cli/src/commands/squash.rs b/cli/src/commands/squash.rs
index 79f13fba31..462fec1e8c 100644
--- a/cli/src/commands/squash.rs
+++ b/cli/src/commands/squash.rs
@@ -13,6 +13,7 @@
 // limitations under the License.
 
 use clap_complete::ArgValueCandidates;
+use clap_complete::ArgValueCompleter;
 use itertools::Itertools as _;
 use jj_lib::commit::Commit;
 use jj_lib::commit::CommitIteratorExt;
@@ -93,7 +94,7 @@ pub(crate) struct SquashArgs {
     #[arg(
         conflicts_with_all = ["interactive", "tool"],
         value_hint = clap::ValueHint::AnyPath,
-        add = ArgValueCandidates::new(complete::squash_revision_files),
+        add = ArgValueCompleter::new(complete::squash_revision_files),
     )]
     paths: Vec<String>,
     /// The source revision will not be abandoned
diff --git a/cli/src/complete.rs b/cli/src/complete.rs
index ed829a50b2..bad1e81504 100644
--- a/cli/src/complete.rs
+++ b/cli/src/complete.rs
@@ -448,7 +448,23 @@ pub fn leaf_config_keys() -> Vec<CompletionCandidate> {
     config_keys_impl(true)
 }
 
-fn all_files_from_rev(rev: String) -> Vec<CompletionCandidate> {
+fn dir_prefix_from<'a>(path: &'a str, current: &str) -> Option<&'a str> {
+    path[current.len()..]
+        .split_once(std::path::MAIN_SEPARATOR)
+        .map(|(next, _)| path.split_at(current.len() + next.len() + 1).0)
+}
+
+fn current_prefix_to_fileset(current: &str) -> String {
+    let cur_esc = glob::Pattern::escape(current);
+    let dir_pat = format!("{cur_esc}*/**");
+    let path_pat = format!("{cur_esc}*");
+    format!("glob:{dir_pat:?} | glob:{path_pat:?}")
+}
+
+fn all_files_from_rev(rev: String, current: &std::ffi::OsStr) -> Vec<CompletionCandidate> {
+    let Some(current) = current.to_str() else {
+        return Vec::new();
+    };
     with_jj(|jj, _| {
         let mut child = jj
             .build()
@@ -456,6 +472,9 @@ fn all_files_from_rev(rev: String) -> Vec<CompletionCandidate> {
             .arg("list")
             .arg("--revision")
             .arg(rev)
+            .arg("--config-toml")
+            .arg("ui.allow-filesets = true")
+            .arg(current_prefix_to_fileset(current))
             .stdout(std::process::Stdio::piped())
             .spawn()
             .map_err(user_error)?;
@@ -465,7 +484,13 @@ fn all_files_from_rev(rev: String) -> Vec<CompletionCandidate> {
             .lines()
             .take(1_000)
             .map_while(Result::ok)
-            .map(CompletionCandidate::new)
+            .map(|path| {
+                if let Some(dir_path) = dir_prefix_from(&path, current) {
+                    return CompletionCandidate::new(dir_path);
+                }
+                CompletionCandidate::new(path)
+            })
+            .dedup() // directories may occur multiple times
             .collect())
     })
 }
@@ -473,8 +498,16 @@ fn all_files_from_rev(rev: String) -> Vec<CompletionCandidate> {
 fn modified_files_from_rev_with_jj_cmd(
     rev: (String, Option<String>),
     mut cmd: std::process::Command,
+    current: &std::ffi::OsStr,
 ) -> Result<Vec<CompletionCandidate>, CommandError> {
-    cmd.arg("diff").arg("--summary");
+    let Some(current) = current.to_str() else {
+        return Ok(Vec::new());
+    };
+    cmd.arg("diff")
+        .arg("--summary")
+        .arg("--config-toml")
+        .arg("ui.allow-filesets = true")
+        .arg(current_prefix_to_fileset(current));
     match rev {
         (rev, None) => cmd.arg("--revision").arg(rev),
         (from, Some(to)) => cmd.arg("--from").arg(from).arg("--to").arg(to),
@@ -488,6 +521,11 @@ fn modified_files_from_rev_with_jj_cmd(
             let (mode, path) = line
                 .split_once(' ')
                 .expect("diff --summary should contain a space between mode and path");
+
+            if let Some(dir_path) = dir_prefix_from(path, current) {
+                return CompletionCandidate::new(dir_path);
+            }
+
             let help = match mode {
                 "M" => "Modified".into(),
                 "D" => "Deleted".into(),
@@ -498,14 +536,21 @@ fn modified_files_from_rev_with_jj_cmd(
             };
             CompletionCandidate::new(path).help(Some(help.into()))
         })
+        .dedup() // directories may occur multiple times
         .collect())
 }
 
-fn modified_files_from_rev(rev: (String, Option<String>)) -> Vec<CompletionCandidate> {
-    with_jj(|jj, _| modified_files_from_rev_with_jj_cmd(rev, jj.build()))
+fn modified_files_from_rev(
+    rev: (String, Option<String>),
+    current: &std::ffi::OsStr,
+) -> Vec<CompletionCandidate> {
+    with_jj(|jj, _| modified_files_from_rev_with_jj_cmd(rev, jj.build(), current))
 }
 
-fn conflicted_files_from_rev(rev: &str) -> Vec<CompletionCandidate> {
+fn conflicted_files_from_rev(rev: &str, current: &std::ffi::OsStr) -> Vec<CompletionCandidate> {
+    let Some(current) = current.to_str() else {
+        return Vec::new();
+    };
     with_jj(|jj, _| {
         let output = jj
             .build()
@@ -513,59 +558,69 @@ fn conflicted_files_from_rev(rev: &str) -> Vec<CompletionCandidate> {
             .arg("--list")
             .arg("--revision")
             .arg(rev)
+            .arg("--config-toml")
+            .arg("ui.allow-filesets = true")
+            .arg(current_prefix_to_fileset(current))
             .output()
             .map_err(user_error)?;
         let stdout = String::from_utf8_lossy(&output.stdout);
 
         Ok(stdout
             .lines()
-            .filter_map(|line| line.split_whitespace().next())
-            .map(CompletionCandidate::new)
+            .map(|line| {
+                let path = line
+                    .split_whitespace()
+                    .next()
+                    .expect("resolve --list should contain whitespace after path");
+
+                if let Some(dir_path) = dir_prefix_from(path, current) {
+                    return CompletionCandidate::new(dir_path);
+                }
+                CompletionCandidate::new(path)
+            })
+            .dedup() // directories may occur multiple times
             .collect())
     })
 }
 
-pub fn modified_files() -> Vec<CompletionCandidate> {
-    modified_files_from_rev(("@".into(), None))
+pub fn modified_files(current: &std::ffi::OsStr) -> Vec<CompletionCandidate> {
+    modified_files_from_rev(("@".into(), None), current)
 }
 
 pub fn all_revision_files(current: &std::ffi::OsStr) -> Vec<CompletionCandidate> {
-    // TODO: Use `current` once `jj file list` gains the ability to list only
-    // the content of the "current" directory.
-    let _ = current;
-    all_files_from_rev(parse::revision_or_wc())
+    all_files_from_rev(parse::revision_or_wc(), current)
 }
 
-pub fn modified_revision_files() -> Vec<CompletionCandidate> {
-    modified_files_from_rev((parse::revision_or_wc(), None))
+pub fn modified_revision_files(current: &std::ffi::OsStr) -> Vec<CompletionCandidate> {
+    modified_files_from_rev((parse::revision_or_wc(), None), current)
 }
 
-pub fn modified_range_files() -> Vec<CompletionCandidate> {
+pub fn modified_range_files(current: &std::ffi::OsStr) -> Vec<CompletionCandidate> {
     match parse::range() {
-        Some((from, to)) => modified_files_from_rev((from, Some(to))),
-        None => modified_files_from_rev(("@".into(), None)),
+        Some((from, to)) => modified_files_from_rev((from, Some(to)), current),
+        None => modified_files_from_rev(("@".into(), None), current),
     }
 }
 
-pub fn modified_revision_or_range_files() -> Vec<CompletionCandidate> {
+pub fn modified_revision_or_range_files(current: &std::ffi::OsStr) -> Vec<CompletionCandidate> {
     if let Some(rev) = parse::revision() {
-        return modified_files_from_rev((rev, None));
+        return modified_files_from_rev((rev, None), current);
     }
-    modified_range_files()
+    modified_range_files(current)
 }
 
-pub fn revision_conflicted_files() -> Vec<CompletionCandidate> {
-    conflicted_files_from_rev(&parse::revision_or_wc())
+pub fn revision_conflicted_files(current: &std::ffi::OsStr) -> Vec<CompletionCandidate> {
+    conflicted_files_from_rev(&parse::revision_or_wc(), current)
 }
 
 /// Specific function for completing file paths for `jj squash`
-pub fn squash_revision_files() -> Vec<CompletionCandidate> {
+pub fn squash_revision_files(current: &std::ffi::OsStr) -> Vec<CompletionCandidate> {
     let rev = parse::squash_revision().unwrap_or_else(|| "@".into());
-    modified_files_from_rev((rev, None))
+    modified_files_from_rev((rev, None), current)
 }
 
 /// Specific function for completing file paths for `jj interdiff`
-pub fn interdiff_files() -> Vec<CompletionCandidate> {
+pub fn interdiff_files(current: &std::ffi::OsStr) -> Vec<CompletionCandidate> {
     let Some((from, to)) = parse::range() else {
         return Vec::new();
     };
@@ -573,8 +628,12 @@ pub fn interdiff_files() -> Vec<CompletionCandidate> {
     // files that are the same in both, which is a false positive. This approach
     // is more lightweight than actually doing a temporary rebase here.
     with_jj(|jj, _| {
-        let mut res = modified_files_from_rev_with_jj_cmd((from, None), jj.build())?;
-        res.extend(modified_files_from_rev_with_jj_cmd((to, None), jj.build())?);
+        let mut res = modified_files_from_rev_with_jj_cmd((from, None), jj.build(), current)?;
+        res.extend(modified_files_from_rev_with_jj_cmd(
+            (to, None),
+            jj.build(),
+            current,
+        )?);
         Ok(res)
     })
 }
diff --git a/cli/tests/test_completion.rs b/cli/tests/test_completion.rs
index 409a3f691f..6f8da88795 100644
--- a/cli/tests/test_completion.rs
+++ b/cli/tests/test_completion.rs
@@ -550,6 +550,9 @@ fn create_commit(
         test_env.jj_cmd_ok(repo_path, &args);
     }
     for (name, content) in files {
+        if let Some((dir, _)) = name.rsplit_once('/') {
+            std::fs::create_dir_all(repo_path.join(dir)).unwrap();
+        }
         match content {
             Some(content) => std::fs::write(repo_path.join(name), content).unwrap(),
             None => std::fs::remove_file(repo_path.join(name)).unwrap(),
@@ -564,6 +567,10 @@ fn test_files() {
     test_env.jj_cmd_ok(test_env.env_root(), &["git", "init", "repo"]);
     let repo_path = test_env.env_root().join("repo");
 
+    // Completions for files use filesets internally.
+    // Ensure they still work if the user has them disabled.
+    test_env.add_config("ui.allow-filesets = false");
+
     create_commit(
         &test_env,
         &repo_path,
@@ -588,6 +595,9 @@ fn test_files() {
             ("f_renamed", Some("renamed\n")),
             ("f_deleted", None),
             ("f_added", Some("added\n")),
+            ("f_dir/dir_file_1", Some("foo\n")),
+            ("f_dir/dir_file_2", Some("foo\n")),
+            ("f_dir/dir_file_3", Some("foo\n")),
         ],
     );
 
@@ -600,6 +610,9 @@ fn test_files() {
         &[
             ("f_modified", Some("modified_again\n")),
             ("f_added_2", Some("added_2\n")),
+            ("f_dir/dir_file_1", Some("bar\n")),
+            ("f_dir/dir_file_2", Some("bar\n")),
+            ("f_dir/dir_file_3", Some("bar\n")),
         ],
     );
     test_env.jj_cmd_ok(&repo_path, &["rebase", "-r=@", "-d=first"]);
@@ -639,20 +652,26 @@ fn test_files() {
     );
 
     let stdout = test_env.jj_cmd_success(&repo_path, &["log", "-r", "all()", "--summary"]);
-    insta::assert_snapshot!(stdout, @r"
-    @  wqnwkozp test.user@example.com 2001-02-03 08:05:20 working_copy 89d772f3
+    insta::assert_snapshot!(stdout.replace('\\', "/"), @r"
+    @  wqnwkozp test.user@example.com 2001-02-03 08:05:20 working_copy 45c3a621
     │  working_copy
     │  A f_added_2
     │  M f_modified
-    ○  zsuskuln test.user@example.com 2001-02-03 08:05:11 second 12ffc2f7
+    ○  zsuskuln test.user@example.com 2001-02-03 08:05:11 second 77a99380
     │  second
     │  A f_added
     │  D f_deleted
+    │  A f_dir/dir_file_1
+    │  A f_dir/dir_file_2
+    │  A f_dir/dir_file_3
     │  M f_modified
     │  A f_renamed
-    │ ×  royxmykx test.user@example.com 2001-02-03 08:05:14 conflicted 14453858 conflict
+    │ ×  royxmykx test.user@example.com 2001-02-03 08:05:14 conflicted 23eb154d conflict
     ├─╯  conflicted
     │    A f_added_2
+    │    A f_dir/dir_file_1
+    │    A f_dir/dir_file_2
+    │    A f_dir/dir_file_3
     │    M f_modified
     ○  rlvkpnrz test.user@example.com 2001-02-03 08:05:09 first 2a2f433c
     │  first
@@ -676,9 +695,10 @@ fn test_files() {
     let test_env = test_env;
 
     let stdout = test_env.jj_cmd_success(&repo_path, &["--", "jj", "file", "show", "f_"]);
-    insta::assert_snapshot!(stdout, @r"
+    insta::assert_snapshot!(stdout.replace('\\', "/"), @r"
     f_added
     f_added_2
+    f_dir/
     f_modified
     f_not_yet_renamed
     f_renamed
@@ -687,27 +707,47 @@ fn test_files() {
 
     let stdout =
         test_env.jj_cmd_success(&repo_path, &["--", "jj", "file", "annotate", "-r@-", "f_"]);
-    insta::assert_snapshot!(stdout, @r"
+    insta::assert_snapshot!(stdout.replace('\\', "/"), @r"
     f_added
+    f_dir/
     f_modified
     f_not_yet_renamed
     f_renamed
     f_unchanged
     ");
-
     let stdout = test_env.jj_cmd_success(&repo_path, &["--", "jj", "diff", "-r", "@-", "f_"]);
-    insta::assert_snapshot!(stdout, @r"
+    insta::assert_snapshot!(stdout.replace('\\', "/"), @r"
     f_added	Added
     f_deleted	Deleted
+    f_dir/
     f_modified	Modified
     f_renamed	Added
     ");
+
+    let stdout = test_env.jj_cmd_success(
+        &repo_path,
+        &[
+            "--",
+            "jj",
+            "diff",
+            "-r",
+            "@-",
+            &format!("f_dir{}", std::path::MAIN_SEPARATOR),
+        ],
+    );
+    insta::assert_snapshot!(stdout.replace('\\', "/"), @r"
+    f_dir/dir_file_1	Added
+    f_dir/dir_file_2	Added
+    f_dir/dir_file_3	Added
+    ");
+
     let stdout = test_env.jj_cmd_success(
         &repo_path,
         &["--", "jj", "diff", "--from", "root()", "--to", "@-", "f_"],
     );
-    insta::assert_snapshot!(stdout, @r"
+    insta::assert_snapshot!(stdout.replace('\\', "/"), @r"
     f_added	Added
+    f_dir/
     f_modified	Added
     f_not_yet_renamed	Added
     f_renamed	Added
@@ -726,7 +766,7 @@ fn test_files() {
             "f_",
         ],
     );
-    insta::assert_snapshot!(stdout, @r"
+    insta::assert_snapshot!(stdout.replace('\\', "/"), @r"
     f_interdiff_only_from	Added
     f_interdiff_same	Added
     f_interdiff_only_to	Added
@@ -735,7 +775,7 @@ fn test_files() {
 
     // squash has a different behavior with --from and --to flags
     let stdout = test_env.jj_cmd_success(&repo_path, &["--", "jj", "squash", "-f=first", "f_"]);
-    insta::assert_snapshot!(stdout, @r"
+    insta::assert_snapshot!(stdout.replace('\\', "/"), @r"
     f_deleted	Added
     f_modified	Added
     f_not_yet_renamed	Added
@@ -744,5 +784,8 @@ fn test_files() {
 
     let stdout =
         test_env.jj_cmd_success(&repo_path, &["--", "jj", "resolve", "-r=conflicted", "f_"]);
-    insta::assert_snapshot!(stdout, @"f_modified");
+    insta::assert_snapshot!(stdout.replace('\\', "/"), @r"
+    f_dir/
+    f_modified
+    ");
 }