diff --git a/docs/next/CHANGELOG.md b/docs/next/CHANGELOG.md
index d854d10b2e..c02f26779c 100644
--- a/docs/next/CHANGELOG.md
+++ b/docs/next/CHANGELOG.md
@@ -17,6 +17,7 @@
 - Windows clients now preserve layout-generated text for Shift-only keys, so characters such as `/` on German keyboards reach shell panes and pasted input. (#3045)
 - Windows panes now keep bare `cursor-agent` launches detected after Cursor hands off to its bundled Node process. (#3032)
 - Oversized Kitty images no longer prevent smaller images shown later in the same pane from rendering. (#3033)
+- `herdr agent explain --file` now reports fixture read failures as structured JSON instead of exposing Rust I/O debug output. (#3022)
 - Claude Code panes now use visible turn, background shell, and background agent activity as working-state fallbacks when OSC titles are unavailable or disabled. (#1630, #2241)
 - Claude Code panes now remain working while MCP tasks continue in the background after a turn ends. (#3090)
 - Tab bar status commands now remove ESC-prefixed terminal control sequences instead of displaying their sequence bodies as text. (#3001)
diff --git a/src/cli/agent.rs b/src/cli/agent.rs
index 306c3bd9fa..42bc5e1cb1 100644
--- a/src/cli/agent.rs
+++ b/src/cli/agent.rs
@@ -2,8 +2,8 @@ use std::time::{Duration, Instant};
 
 use crate::api::schema::{
     AgentPromptParams, AgentPromptWaitOptions, AgentReadParams, AgentRenameParams,
-    AgentSendKeysParams, AgentStartParams, AgentTarget, AgentWaitParams, EmptyParams, Method,
-    PaneProcessInfoParams, PaneTarget, ReadFormat, ReadSource, Request,
+    AgentSendKeysParams, AgentStartParams, AgentTarget, AgentWaitParams, EmptyParams, ErrorBody,
+    ErrorResponse, Method, PaneProcessInfoParams, PaneTarget, ReadFormat, ReadSource, Request,
 };
 
 const AGENT_START_POLL_INTERVAL: Duration = Duration::from_millis(100);
@@ -118,7 +118,21 @@ fn agent_explain(args: &[String]) -> std::io::Result<i32> {
             eprintln!("herdr agent explain --file requires --agent LABEL");
             return Ok(2);
         };
-        let content = std::fs::read_to_string(path)?;
+        let content = match std::fs::read_to_string(&path) {
+            Ok(content) => content,
+            Err(err) => {
+                let response = ErrorResponse {
+                    id: "cli:agent:explain".into(),
+                    error: ErrorBody {
+                        code: "agent_explain_file_read_failed".into(),
+                        message: format!("failed to read agent explain file {path}: {err}"),
+                    },
+                };
+                let response = serde_json::to_string(&response).map_err(std::io::Error::other)?;
+                eprintln!("{response}");
+                return Ok(1);
+            }
+        };
         crate::detect::manifest::explain_to_json_value(&crate::detect::manifest::explain_for_label(
             &agent_label,
             &content,
diff --git a/tests/cli/agents.rs b/tests/cli/agents.rs
index 3164b8021b..c3e98f86f4 100644
--- a/tests/cli/agents.rs
+++ b/tests/cli/agents.rs
@@ -1,5 +1,34 @@
 use super::harness::*;
 
+#[test]
+fn agent_explain_missing_file_reports_json_error() {
+    let base = unique_test_dir();
+    let missing = base.join("missing-screen.txt");
+    let output = run_named_cli(
+        &base.join("config"),
+        &base.join("runtime"),
+        &[
+            "agent",
+            "explain",
+            "--file",
+            missing.to_str().unwrap(),
+            "--agent",
+            "claude",
+            "--json",
+        ],
+    );
+
+    assert_eq!(output.status.code(), Some(1));
+    assert!(output.stdout.is_empty());
+    let error: serde_json::Value = serde_json::from_slice(&output.stderr).unwrap();
+    assert_eq!(error["id"], "cli:agent:explain");
+    assert_eq!(error["error"]["code"], "agent_explain_file_read_failed");
+    assert!(error["error"]["message"]
+        .as_str()
+        .unwrap()
+        .contains(missing.to_str().unwrap()));
+}
+
 fn write_delayed_shell_and_fake_pi(
     base: &Path,
     shell_delay_seconds: &str,