diff --git a/docker/Dockerfile.base b/docker/Dockerfile.base
index 23ad9813..03093569 100644
--- a/docker/Dockerfile.base
+++ b/docker/Dockerfile.base
@@ -33,7 +33,12 @@ RUN apt-get update && apt-get install -y --no-install-recommends \
     && rm -rf /var/lib/apt/lists/*
 
 # Copy the huskies binary and entrypoint from the main image.
-COPY --from=huskies-src /usr/local/bin/huskies /usr/local/bin/huskies
+# The binary lives in /opt/huskies/bin (chowned to the huskies user below) so
+# the in-process upgrade path (`POST /api/upgrade`) can atomically replace it
+# without root: rename() needs write permission on the *directory*, not just
+# the file. /usr/local/bin/huskies stays a symlink so PATH resolution and the
+# entrypoint CMD are unchanged.
+COPY --from=huskies-src /usr/local/bin/huskies /opt/huskies/bin/huskies
 COPY --from=huskies-src /usr/local/bin/entrypoint.sh /usr/local/bin/entrypoint.sh
 
 # Non-root user — Claude Code refuses --dangerously-skip-permissions as root.
@@ -44,6 +49,8 @@ RUN groupadd -r huskies \
     && mkdir -p /home/huskies/.ssh \
     && chmod 700 /home/huskies/.ssh \
     && chown -R huskies:huskies /home/huskies \
+    && chown -R huskies:huskies /opt/huskies \
+    && ln -s /opt/huskies/bin/huskies /usr/local/bin/huskies \
     && mkdir -p /workspace \
     && chown huskies:huskies /workspace \
     && git config --global init.defaultBranch master \
diff --git a/server/src/upgrade.rs b/server/src/upgrade.rs
index a78aacca..32aaa996 100644
--- a/server/src/upgrade.rs
+++ b/server/src/upgrade.rs
@@ -94,9 +94,22 @@ pub async fn run_cli_upgrade(source_url: &str, target: &Path) -> Result<(), Stri
 
 // ── Helpers ───────────────────────────────────────────────────────────────
 
-/// Resolve the path to replace: `current_exe()` if accessible, else
-/// `/usr/local/bin/huskies`.
+/// Resolve the path to replace with the new binary.
+///
+/// Inside project containers the binary is installed at
+/// `/opt/huskies/bin/huskies` (a huskies-owned directory, so the atomic
+/// tmp-write + rename works without root) and `/usr/local/bin/huskies` is a
+/// symlink to it.  That path is preferred over `current_exe()` because
+/// `current_exe()` can point at a stale location — e.g.
+/// `/workspace/target/release/huskies` after a historical in-container
+/// rebuild — which the entrypoint would never launch after a restart.
+///
+/// Outside containers (no `/opt/huskies`), falls back to `current_exe()`.
 pub fn resolve_target_path() -> PathBuf {
+    let container_path = PathBuf::from("/opt/huskies/bin/huskies");
+    if container_path.exists() {
+        return container_path;
+    }
     std::env::current_exe().unwrap_or_else(|_| PathBuf::from("/usr/local/bin/huskies"))
 }