diff --git a/server/jetty/src/main/java/io/deephaven/server/jetty/JettyBackedGrpcServer.java b/server/jetty/src/main/java/io/deephaven/server/jetty/JettyBackedGrpcServer.java
index 19acd0acc55..8ba0eb5abc0 100644
--- a/server/jetty/src/main/java/io/deephaven/server/jetty/JettyBackedGrpcServer.java
+++ b/server/jetty/src/main/java/io/deephaven/server/jetty/JettyBackedGrpcServer.java
@@ -29,6 +29,8 @@
 import org.eclipse.jetty.server.Server;
 import org.eclipse.jetty.server.ServerConnector;
 import org.eclipse.jetty.server.SslConnectionFactory;
+import org.eclipse.jetty.server.handler.HandlerCollection;
+import org.eclipse.jetty.servlet.DefaultServlet;
 import org.eclipse.jetty.servlet.ErrorPageErrorHandler;
 import org.eclipse.jetty.servlet.FilterHolder;
 import org.eclipse.jetty.util.resource.Resource;
@@ -49,7 +51,7 @@
 
 import static io.grpc.servlet.web.websocket.MultiplexedWebSocketServerStream.GRPC_WEBSOCKETS_MULTIPLEX_PROTOCOL;
 import static io.grpc.servlet.web.websocket.WebSocketServerStream.GRPC_WEBSOCKETS_PROTOCOL;
-import static org.eclipse.jetty.servlet.ServletContextHandler.SESSIONS;
+import static org.eclipse.jetty.servlet.ServletContextHandler.NO_SESSIONS;
 
 public class JettyBackedGrpcServer implements GrpcServer {
 
@@ -63,7 +65,7 @@ public JettyBackedGrpcServer(
         jetty.addConnector(createConnector(jetty, config));
 
         final WebAppContext context =
-                new WebAppContext(null, "/", null, null, null, new ErrorPageErrorHandler(), SESSIONS);
+                new WebAppContext(null, "/", null, null, null, new ErrorPageErrorHandler(), NO_SESSIONS);
         try {
             String knownFile = "/ide/index.html";
             URL ide = JettyBackedGrpcServer.class.getResource(knownFile);
@@ -72,6 +74,7 @@ public JettyBackedGrpcServer(
         } catch (IOException ioException) {
             throw new UncheckedIOException(ioException);
         }
+        context.setInitParameter(DefaultServlet.CONTEXT_INIT + "dirAllowed", "false");
 
         // For the Web UI, cache everything in the static folder
         // https://create-react-app.dev/docs/production-build/#static-file-caching
@@ -85,9 +88,6 @@ public JettyBackedGrpcServer(
         // Add an extra filter to redirect from / to /ide/
         context.addFilter(HomeFilter.class, "/", EnumSet.noneOf(DispatcherType.class));
 
-        // Direct jetty all use this configuration as the root application
-        context.setContextPath("/");
-
         // Handle grpc-web connections, translate to vanilla grpc
         context.addFilter(new FilterHolder(new GrpcWebFilter()), "/*", EnumSet.noneOf(DispatcherType.class));
 
@@ -123,7 +123,14 @@ public <T> T getEndpointInstance(Class<T> endpointClass) throws InstantiationExc
                 );
             });
         }
-        jetty.setHandler(context);
+
+        // Note: handler order matters due to pathSpec order
+        HandlerCollection handlers = new HandlerCollection();
+        // Set up /js-plugins/*
+        JsPlugins.maybeAdd(handlers::addHandler);
+        // Set up /*
+        handlers.addHandler(context);
+        jetty.setHandler(handlers);
     }
 
     @Override
diff --git a/server/jetty/src/main/java/io/deephaven/server/jetty/JsPlugins.java b/server/jetty/src/main/java/io/deephaven/server/jetty/JsPlugins.java
new file mode 100644
index 00000000000..f2ec9b2fe77
--- /dev/null
+++ b/server/jetty/src/main/java/io/deephaven/server/jetty/JsPlugins.java
@@ -0,0 +1,40 @@
+package io.deephaven.server.jetty;
+
+import io.deephaven.configuration.Configuration;
+import org.eclipse.jetty.security.ConstraintSecurityHandler;
+import org.eclipse.jetty.server.Handler;
+import org.eclipse.jetty.servlet.DefaultServlet;
+import org.eclipse.jetty.servlet.ErrorPageErrorHandler;
+import org.eclipse.jetty.util.resource.Resource;
+import org.eclipse.jetty.webapp.WebAppContext;
+
+import java.io.IOException;
+import java.io.UncheckedIOException;
+import java.util.function.Consumer;
+
+import static org.eclipse.jetty.servlet.ServletContextHandler.NO_SESSIONS;
+
+class JsPlugins {
+
+    public static void maybeAdd(Consumer<Handler> addHandler) {
+        // Note: this would probably be better to live in JettyConfig - but until we establish more formal expectations
+        // for js plugin configuration and workflows, we'll keep this here.
+        final String resourceBase =
+                Configuration.getInstance().getStringWithDefault("deephaven.jsPlugins.resourceBase", null);
+        if (resourceBase == null) {
+            return;
+        }
+        try {
+            Resource resource = ControlledCacheResource.wrap(Resource.newResource(resourceBase));
+            WebAppContext context =
+                    new WebAppContext(null, "/js-plugins/", null, null, null, new ErrorPageErrorHandler(), NO_SESSIONS);
+            context.setBaseResource(resource);
+            context.setInitParameter(DefaultServlet.CONTEXT_INIT + "dirAllowed", "false");
+            // Suppress warnings about security handlers
+            context.setSecurityHandler(new ConstraintSecurityHandler());
+            addHandler.accept(context);
+        } catch (IOException e) {
+            throw new IllegalStateException(String.format("Unable to resolve resourceBase '%s'", resourceBase), e);
+        }
+    }
+}