diff --git a/services/git-bridge/src/main/java/uk/ac/ic/wlgitbridge/server/GitBridgeServer.java b/services/git-bridge/src/main/java/uk/ac/ic/wlgitbridge/server/GitBridgeServer.java
index 5a1e199b32..1150b4a642 100644
--- a/services/git-bridge/src/main/java/uk/ac/ic/wlgitbridge/server/GitBridgeServer.java
+++ b/services/git-bridge/src/main/java/uk/ac/ic/wlgitbridge/server/GitBridgeServer.java
@@ -123,6 +123,9 @@ public class GitBridgeServer {
         handlers.addHandler(new DefaultHandler());
 
         api.setHandler(handlers);
+
+        ProductionErrorHandler errorHandler = new ProductionErrorHandler();
+        api.setErrorHandler(errorHandler);
         return api;
     }
 
@@ -149,6 +152,8 @@ public class GitBridgeServer {
                 ),
                 "/*"
         );
+        ProductionErrorHandler errorHandler = new ProductionErrorHandler();
+        servletContextHandler.setErrorHandler(errorHandler);
         return servletContextHandler;
     }
 
diff --git a/services/git-bridge/src/main/java/uk/ac/ic/wlgitbridge/server/ProductionErrorHandler.java b/services/git-bridge/src/main/java/uk/ac/ic/wlgitbridge/server/ProductionErrorHandler.java
new file mode 100644
index 0000000000..d4b19e26fe
--- /dev/null
+++ b/services/git-bridge/src/main/java/uk/ac/ic/wlgitbridge/server/ProductionErrorHandler.java
@@ -0,0 +1,21 @@
+package uk.ac.ic.wlgitbridge.server;
+
+import javax.servlet.http.HttpServletRequest;
+import javax.servlet.http.HttpServletResponse;
+import org.eclipse.jetty.server.handler.ErrorHandler;
+import java.io.IOException;
+
+public class ProductionErrorHandler extends ErrorHandler {
+    @Override
+    public void handle(
+    		String target, 
+    		org.eclipse.jetty.server.Request baseRequest, 
+    		HttpServletRequest request, 
+    		HttpServletResponse response
+    	) throws IOException {
+	        response.getWriter()
+	            .append("{\"message\":\"HTTP error ")
+	            .append(String.valueOf(response.getStatus()))
+	            .append("\"}");
+    	}
+}
diff --git a/services/git-bridge/src/test/java/uk/ac/ic/wlgitbridge/application/WLGitBridgeIntegrationTest.java b/services/git-bridge/src/test/java/uk/ac/ic/wlgitbridge/application/WLGitBridgeIntegrationTest.java
index cc5a726cc6..20b1fb85ed 100644
--- a/services/git-bridge/src/test/java/uk/ac/ic/wlgitbridge/application/WLGitBridgeIntegrationTest.java
+++ b/services/git-bridge/src/test/java/uk/ac/ic/wlgitbridge/application/WLGitBridgeIntegrationTest.java
@@ -693,6 +693,40 @@ public class WLGitBridgeIntegrationTest {
         wlgb.stop();
     }
 
+    @Test
+    public void usesCustomErrorHandler(
+    ) throws IOException, ExecutionException, InterruptedException {
+
+        int gitBridgePort = 33873;
+        int mockServerPort = 3873;
+
+        MockSnapshotServer server = new MockSnapshotServer(
+                mockServerPort, getResource("/canServePushedFiles").toFile());
+        server.start();
+        server.setState(states.get("canServePushedFiles").get("state"));
+
+        GitBridgeApp wlgb = new GitBridgeApp(new String[] {
+                makeConfigFile(gitBridgePort, mockServerPort)
+        });
+        wlgb.run();
+
+        // With an invalid project and no key, we should get a 404,
+        // which is rendered by our custom error handler.
+        String url = "http://127.0.0.1:" + gitBridgePort + "/api/notavalidproject/main.tex";
+        Response response = new AsyncHttpClient().prepareGet(url).execute().get();
+        assertEquals(404, response.getStatusCode());
+        assertEquals("{\"message\":\"HTTP error 404\"}", response.getResponseBody());
+
+        // With an unsupported URL outside the api, we should get a 500,
+        // which is rendered by our custom error handler.
+        url = "http://127.0.0.1:" + gitBridgePort + "/foo";
+        response = new AsyncHttpClient().prepareGet(url).execute().get();
+        assertEquals(500, response.getStatusCode());
+        assertEquals("{\"message\":\"HTTP error 500\"}", response.getResponseBody());
+
+        wlgb.stop();
+    }
+
     private String makeConfigFile(
             int port,
             int apiPort