diff --git a/gix-discover/src/is.rs b/gix-discover/src/is.rs
index 57dcda9338a..a09c7d9ec40 100644
--- a/gix-discover/src/is.rs
+++ b/gix-discover/src/is.rs
@@ -106,7 +106,7 @@ pub(crate) fn git_with_metadata(
         let worktree_and_common_dir = crate::path::from_plain_file(&common_dir)
             .and_then(Result::ok)
             .and_then(|cd| {
-                crate::path::from_plain_file(&dot_git.join("gitdir"))
+                crate::path::from_plain_file_relative_to_file(&dot_git.join("gitdir"))
                     .and_then(Result::ok)
                     .map(|worktree_gitfile| (crate::path::without_dot_git_dir(worktree_gitfile), cd))
             });
diff --git a/gix-discover/src/path.rs b/gix-discover/src/path.rs
index e783c656a40..674bacfc324 100644
--- a/gix-discover/src/path.rs
+++ b/gix-discover/src/path.rs
@@ -44,6 +44,30 @@ fn read_regular_file_content_with_size_limit(path: &std::path::Path) -> std::io:
     Ok(buf)
 }
 
+/// Read a plain path file, returning `None` if the file is missing.
+///
+/// Linked-worktree `gitdir` files are plain path files in Git, not `gitdir:`
+/// files. Match Git's `get_linked_worktree()` behavior by trimming trailing
+/// whitespace before interpreting the content. Empty or whitespace-only path
+/// files are invalid.
+fn read_plain_file_content(path: &std::path::Path) -> Option<std::io::Result<Vec<u8>>> {
+    use bstr::ByteSlice;
+    let mut buf = match read_regular_file_content_with_size_limit(path) {
+        Ok(buf) => buf,
+        Err(err) if err.kind() == std::io::ErrorKind::NotFound => return None,
+        Err(err) => return Some(Err(err)),
+    };
+    let trimmed_len = buf.trim_end().len();
+    buf.truncate(trimmed_len);
+    if buf.is_empty() {
+        return Some(Err(std::io::Error::new(
+            std::io::ErrorKind::InvalidData,
+            format!("Refusing to read an empty path from '{}'", path.display()),
+        )));
+    }
+    Some(Ok(buf))
+}
+
 /// Guess the kind of repository by looking at its `git_dir` path and return it.
 /// Return `None` if `git_dir` isn't called `.git` or isn't within `.git/worktrees` or `.git/modules`, or if it's
 /// a `.git` suffix like in `foo.git`.
@@ -74,15 +98,21 @@ pub fn repository_kind(git_dir: &Path) -> Option<RepositoryKind> {
 
 /// Reads a plain path from a file that contains it as its only content, with trailing newlines trimmed.
 pub fn from_plain_file(path: &std::path::Path) -> Option<std::io::Result<PathBuf>> {
-    use bstr::ByteSlice;
-    let mut buf = match read_regular_file_content_with_size_limit(path) {
-        Ok(buf) => buf,
-        Err(err) if err.kind() == std::io::ErrorKind::NotFound => return None,
-        Err(err) => return Some(Err(err)),
-    };
-    let trimmed_len = buf.trim_end().len();
-    buf.truncate(trimmed_len);
-    Some(Ok(gix_path::from_bstring(buf)))
+    read_plain_file_content(path).map(|res| res.map(gix_path::from_bstring))
+}
+
+/// Reads a plain path from a file like [`from_plain_file()`], resolving relative paths against
+/// the file's containing directory as needed.
+pub fn from_plain_file_relative_to_file(path: &std::path::Path) -> Option<std::io::Result<PathBuf>> {
+    read_plain_file_content(path).map(|res| {
+        res.map(|buf| {
+            let plain_path = gix_path::from_bstring(buf);
+            match (plain_path.is_relative(), path.parent()) {
+                (true, Some(parent)) => parent.join(plain_path),
+                _ => plain_path,
+            }
+        })
+    })
 }
 
 /// Reads typical `gitdir: ` files from disk as used by worktrees and submodules.
diff --git a/gix-discover/tests/discover/path.rs b/gix-discover/tests/discover/path.rs
index 1f48a7e24ab..8412abc2f07 100644
--- a/gix-discover/tests/discover/path.rs
+++ b/gix-discover/tests/discover/path.rs
@@ -44,6 +44,70 @@ mod from_git_dir_file {
     }
 }
 
+mod from_plain_file_relative_to_file {
+    use crate::path::plain_file_with_content;
+    use std::path::{Path, PathBuf};
+
+    #[test]
+    fn relative_path_is_made_absolute_relative_to_containing_dir() -> crate::Result {
+        let (path, plain_file) = write_and_read(b"relative/path\n")?;
+        assert_eq!(path, plain_file.parent().unwrap().join(Path::new("relative/path")));
+        Ok(())
+    }
+
+    #[test]
+    fn empty_or_whitespace_only_path_is_invalid() -> crate::Result {
+        for content in [b"".as_slice(), b"   \n".as_slice()] {
+            let file = plain_file_with_content(content)?;
+            let err = gix_discover::path::from_plain_file_relative_to_file(file.path())
+                .expect("file exists")
+                .expect_err("empty paths must be rejected");
+            assert_eq!(
+                err.kind(),
+                std::io::ErrorKind::InvalidData,
+                "empty plain path files are malformed, just like in Git"
+            );
+        }
+        Ok(())
+    }
+
+    fn write_and_read(content: &[u8]) -> crate::Result<(PathBuf, PathBuf)> {
+        let file = plain_file_with_content(content)?;
+        Ok((
+            gix_discover::path::from_plain_file_relative_to_file(file.path())
+                .expect("file exists")
+                .expect("valid plain path"),
+            file.path().into(),
+        ))
+    }
+}
+
+mod from_plain_file {
+    use crate::path::plain_file_with_content;
+
+    #[test]
+    fn empty_or_whitespace_only_path_is_invalid() -> crate::Result {
+        for content in [b"".as_slice(), b"   \n".as_slice()] {
+            let file = plain_file_with_content(content)?;
+            let err = gix_discover::path::from_plain_file(file.path())
+                .expect("file exists")
+                .expect_err("empty paths must be rejected");
+            assert_eq!(
+                err.kind(),
+                std::io::ErrorKind::InvalidData,
+                "empty plain path files are malformed, just like in Git"
+            );
+        }
+        Ok(())
+    }
+}
+
+fn plain_file_with_content(content: &[u8]) -> std::io::Result<tempfile::NamedTempFile> {
+    let mut file = tempfile::NamedTempFile::new()?;
+    std::io::Write::write_all(&mut file, content)?;
+    Ok(file)
+}
+
 #[test]
 fn repository_kind() {
     use gix_discover::path::{RepositoryKind::*, repository_kind};
diff --git a/gix-discover/tests/discover/upwards/mod.rs b/gix-discover/tests/discover/upwards/mod.rs
index f5583d2cfe3..5ad0623ce7f 100644
--- a/gix-discover/tests/discover/upwards/mod.rs
+++ b/gix-discover/tests/discover/upwards/mod.rs
@@ -235,6 +235,66 @@ fn from_existing_worktree() -> crate::Result {
     Ok(())
 }
 
+#[test]
+fn from_existing_worktree_with_relative_linking_files() -> crate::Result {
+    let fixture = gix_testtools::scripted_fixture_read_only_needs_archive("make_worktree_relative_linking.sh")?;
+    let main = fixture.join("main");
+    let linked = fixture.join("linked");
+    let private_git_dir = main.join(".git/worktrees/linked");
+    assert_eq!(
+        std::fs::read_to_string(linked.join(".git"))?,
+        "gitdir: ../main/.git/worktrees/linked\n",
+        "the linked checkout uses a relative gitdir file"
+    );
+    let backlink = std::fs::read_to_string(private_git_dir.join("gitdir"))?;
+    assert_eq!(
+        backlink, "../../../../linked/.git\n",
+        "the private git dir points back to the checkout with a relative path"
+    );
+
+    for discover_path in [&linked, &private_git_dir] {
+        let (path, trust) = gix_discover::upwards(discover_path)?;
+        assert_eq!(trust, expected_trust());
+        let (actual_git_dir, actual_worktree) = path.into_repository_and_work_tree_directories();
+        assert_eq!(
+            gix_path::realpath(&actual_git_dir)?,
+            gix_path::realpath(&private_git_dir)?,
+            "discovery resolves the private git dir from relative worktree metadata"
+        );
+        assert_eq!(
+            actual_worktree.as_deref().map(gix_path::realpath).transpose()?,
+            Some(gix_path::realpath(&linked)?),
+            "discovery resolves the linked worktree from relative worktree metadata"
+        );
+    }
+
+    Ok(())
+}
+
+#[test]
+#[cfg(unix)]
+fn from_symlinked_worktree_with_relative_linking_files() -> crate::Result {
+    let fixture = gix_testtools::scripted_fixture_read_only_needs_archive("make_worktree_relative_linking.sh")?;
+    let main = fixture.join("actual/main");
+    let linked_symlink = fixture.join("linked-symlink");
+
+    let (path, trust) = gix_discover::upwards(&linked_symlink)?;
+    assert_eq!(trust, expected_trust());
+    let (actual_git_dir, actual_worktree) = path.into_repository_and_work_tree_directories();
+    assert_eq!(
+        gix_path::realpath(&actual_git_dir)?,
+        gix_path::realpath(main.join(".git/worktrees/linked"))?,
+        "the private git dir is found through a relative gitdir file reached via a symlinked checkout"
+    );
+    assert_eq!(
+        actual_worktree.as_deref(),
+        Some(linked_symlink.as_path()),
+        "the discovered worktree remains the user-provided symlinked checkout"
+    );
+
+    Ok(())
+}
+
 #[cfg(target_os = "macos")]
 #[test]
 fn cross_fs() -> crate::Result {
diff --git a/gix-discover/tests/fixtures/generated-archives/make_worktree_relative_linking.tar b/gix-discover/tests/fixtures/generated-archives/make_worktree_relative_linking.tar
new file mode 100644
index 00000000000..5a11d963e52
Binary files /dev/null and b/gix-discover/tests/fixtures/generated-archives/make_worktree_relative_linking.tar differ
diff --git a/gix-discover/tests/fixtures/make_worktree_relative_linking.sh b/gix-discover/tests/fixtures/make_worktree_relative_linking.sh
new file mode 100755
index 00000000000..3ce37247680
--- /dev/null
+++ b/gix-discover/tests/fixtures/make_worktree_relative_linking.sh
@@ -0,0 +1,21 @@
+#!/usr/bin/env bash
+set -eu -o pipefail
+
+make_repo_with_relative_worktree_links() {
+  local base=$1
+
+  mkdir -p "$base"
+  git -C "$base" init -q main
+  (
+    cd "$base/main"
+    git commit -q --allow-empty -m init
+    git worktree add -q --detach --relative-paths ../linked HEAD
+  )
+}
+
+make_repo_with_relative_worktree_links .
+make_repo_with_relative_worktree_links actual
+
+# The symlinked checkout variant is only used by Unix tests. On platforms where
+# creating symlinks is unavailable, keep the rest of the fixture useful.
+ln -s actual/linked linked-symlink 2>/dev/null || true
diff --git a/gix/src/worktree/proxy.rs b/gix/src/worktree/proxy.rs
index 222fb2685d9..dd7cd856d0c 100644
--- a/gix/src/worktree/proxy.rs
+++ b/gix/src/worktree/proxy.rs
@@ -47,7 +47,7 @@ impl Proxy<'_> {
     /// Note that the location might not exist.
     pub fn base(&self) -> std::io::Result<PathBuf> {
         let git_dir = self.git_dir.join("gitdir");
-        let base_dot_git = gix_discover::path::from_plain_file(&git_dir).ok_or_else(|| {
+        let base_dot_git = gix_discover::path::from_plain_file_relative_to_file(&git_dir).ok_or_else(|| {
             std::io::Error::new(
                 std::io::ErrorKind::NotFound,
                 format!("Required file '{}' does not exist", git_dir.display()),
diff --git a/gix/tests/fixtures/generated-archives/make_worktree_relative_linking.tar b/gix/tests/fixtures/generated-archives/make_worktree_relative_linking.tar
new file mode 100644
index 00000000000..3a4ed0d4596
Binary files /dev/null and b/gix/tests/fixtures/generated-archives/make_worktree_relative_linking.tar differ
diff --git a/gix/tests/fixtures/make_worktree_relative_linking.sh b/gix/tests/fixtures/make_worktree_relative_linking.sh
new file mode 100755
index 00000000000..74c07ec801d
--- /dev/null
+++ b/gix/tests/fixtures/make_worktree_relative_linking.sh
@@ -0,0 +1,21 @@
+#!/usr/bin/env bash
+set -eu -o pipefail
+
+make_repo_with_relative_worktree_links() {
+  local base=$1
+
+  mkdir -p "$base"
+  git -C "$base" init -q main
+  (
+    cd "$base/main"
+    git commit -q --allow-empty -m init
+    git worktree add -q --detach --relative-paths ../linked HEAD
+  )
+}
+
+make_repo_with_relative_worktree_links .
+make_repo_with_relative_worktree_links actual
+
+# The symlinked main-repository variant is only used by Unix tests. On platforms
+# where creating symlinks is unavailable, keep the rest of the fixture useful.
+ln -s actual/main main-symlink 2>/dev/null || true
diff --git a/gix/tests/gix/repository/worktree.rs b/gix/tests/gix/repository/worktree.rs
index 94624f73aa1..10554cdc2f8 100644
--- a/gix/tests/gix/repository/worktree.rs
+++ b/gix/tests/gix/repository/worktree.rs
@@ -261,6 +261,58 @@ fn from_nonbare_parent_repo() {
     run_assertions(repo, false /* bare */);
 }
 
+#[test]
+fn linked_worktree_proxy_base_with_relative_linking_files() -> crate::Result {
+    let fixture = gix_testtools::scripted_fixture_read_only_needs_archive("make_worktree_relative_linking.sh")?;
+    let main = fixture.join("main");
+    let linked = fixture.join("linked");
+    let private_git_dir = main.join(".git/worktrees/linked");
+    let repo = gix::open(&main)?;
+    let worktrees = repo.worktrees()?;
+    assert_eq!(worktrees.len(), 1, "the relative-path fixture has one linked worktree");
+    let proxy = worktrees.into_iter().next().expect("one worktree");
+
+    assert_eq!(
+        gix_path::realpath(proxy.base()?)?,
+        gix_path::realpath(&linked)?,
+        "proxy bases resolve relative worktrees/<id>/gitdir paths against the private git dir"
+    );
+    let linked_repo = proxy.into_repo()?;
+    assert_eq!(
+        linked_repo.workdir().map(gix_path::realpath).transpose()?,
+        Some(gix_path::realpath(&linked)?)
+    );
+    assert_eq!(linked_repo.git_dir(), private_git_dir);
+
+    Ok(())
+}
+
+#[test]
+#[cfg(unix)]
+fn linked_worktree_proxy_base_with_symlinked_main_repo() -> crate::Result {
+    let fixture = gix_testtools::scripted_fixture_read_only_needs_archive("make_worktree_relative_linking.sh")?;
+    let linked = fixture.join("actual/linked");
+    let main_symlink = fixture.join("main-symlink");
+
+    let repo = gix::open(&main_symlink)?;
+    let worktrees = repo.worktrees()?;
+    assert_eq!(worktrees.len(), 1, "the relative-path fixture has one linked worktree");
+    let proxy = worktrees.into_iter().next().expect("one worktree");
+
+    assert_eq!(
+        gix_path::realpath(proxy.base()?)?,
+        gix_path::realpath(&linked)?,
+        "proxy bases preserve symlink semantics when resolving relative worktrees/<id>/gitdir paths"
+    );
+    let repo = proxy.into_repo()?;
+    assert_eq!(
+        repo.workdir().map(gix_path::realpath).transpose()?,
+        Some(gix_path::realpath(&linked)?)
+    );
+
+    Ok(())
+}
+
 #[test]
 fn from_nonbare_parent_repo_set_workdir() -> gix_testtools::Result {
     if gix_testtools::should_skip_as_git_version_is_smaller_than(2, 31, 0) {